ORNITOLOGIA NEOTROPICAL 23: 85–100, 2012 © The Neotropical Ornithological Society

POLLINATION NETWORK OF A COMMU- NITY (TROCHILIDAE, PHAETHORNITHINAE) AND THEIR NECTAR RESOURCES IN THE COLOMBIAN AMAZON

Claudia Rodríguez-Flores1,4, F. Gary Stiles2 & María del Coro Arizmendi3

1 Departamento de Biología, Universidad Nacional de , Bogotá, Colombia. E-mail: [email protected] 2 Instituto de Ciencias Naturales, Universidad Nacional de Colombia, A. A. 7495 Bogotá, Colombia. E-mail: [email protected] 3 Laboratorio de Ecología, UBIPRO, FES-Iztacala, Universidad Nacional Autónoma de México, Av. De los Barrios s/n, Los Reyes Iztacala, Tlalnepantla de Baz, Estado de México, México, C.P. 54090. E-mail: [email protected] 4 Dirección actual: Laboratorio de Ecología, UBIPRO, FES-Iztacala, Universidad Nacional Autónoma de México, Av. De los Barrios s/n, Los Reyes Iztacala, Tlalnepantla de Baz, Es- tado de México, México, C.P. 54090. E-mail: [email protected]

Resumen. – Red de polinización de una comunidad de colibríes ermitaños (Trochilidae: Phaethorni- thinae) y sus recursos de néctar en la amazonia colombiana. - Los colibríes (Aves: Trochilidae) y sus recursos de néctar interactúan construyendo redes de polinización de diferentes grados de complejidad, donde una especie de colibrí puede estar conectada con una o más especies de plantas (o viceversa). En este tra- bajo evaluamos la estructura del ensamblaje de una comunidad de colibríes ermitaños (Subfamilia Phaetho- rnithinae) y las plantas de las que se alimentan, en bosques de la amazonia colombiana. La composición de especies de colibríes se estableció a partir de capturas con redes de niebla y observaciones directas, mientras que el ensamblaje de plantas visitadas por estos se determinó a partir de cargas de polen y observaciones directas. Esta red de polinización está compuesta por siete especies de colibríes y 44 especies de plantas; presenta una estructura asimétrica y está fuertemente anidada. Cuatro de las especies de colibríes fueron altamente generalistas y se alimentaron de un gran número de especies de plantas, mientras que las especies más especialistas de colibríes interactuaron a su vez tanto con especies de plantas tanto generalistas como especialistas. Las interacciones más fuertes entre grupos de colibríes con ciertos grupos de plantas, apoyaron la hipótesis de la coevolución difusa como mecanismo modelador de las interacciones en esta comunidad.

Abstract. - network of a hermit hummingbird community (Trochilidae, Phaethornithinae) and their nectar resources in the Colombian Amazon. – (Aves: Trochilidae) and their nectar resources interact building pollination networks that differs in complexity because co-occurring hummingbirds visit the same and different species..In this work we evaluated the network structure of a hermit hummingbird community (Subfamily Phaethornithinae) and their food resources in a Colombian Amazon for- est. We studied the hummingbird community using mist nets and direct observations, and the plant community with pollen loads and direct observations. This pollination network is composed of seven hummingbird spe- cies and 44 plant species. It has an asymmetric structure and is strongly nested. Four hummingbird species were extremely generalist. Each visited many plant species, while the more specialist hummingbird species interacted with generalist and specialist´s plant species. The strongest interactions between hummingbird’s species groups and some plant’s species groups supports the hypothesis of diffuse co-evolution, where some hummingbirds interact more strongly with some plant species, like modeler of the interactions in this community.

Key words: Amazonas, community organization, diffuse co-evolution, Colombia, hermit hummingbird-flower interaction, mutualistic networks, Phaethornithinae, Trochilidae.

85 85 Rodríguez-Flores et al. CHILEAN PASSERINE SEASONAL BODY MASS

INTRODUCTION (Schuchmann 1999, Arizmendi & Ro- dríguez-Flores 2012). Hermit hummingbirds Ecological communities are formed by inter- (Subfamily Phaethornithinae) have long and actions that include predation, competition curved bills, are mostly understory trapliners and mutualisms such as pollination. They cre- (Stiles & Wolf 1979, Stiles 1981, 1985, Cot- ate a complex network of interacting species ton 1998b, Hilty & Brown 2001), and reach that vary in their connections and the strength their higher dominance and diversity in humid of their interactions. (Verdú & Valiente-Ban- lowland (lower than 1000 m.a.s.l.) in uet 2008, Thompson & Medel 2010). Mutu- the Amazon region (Stiles 1981). These hum- alistic interactions needed for pollination and mingbirds are known as of mono- seed dispersal involve many species that form cot plants especially of the , in complex networks of interdependences (Bas- which they share distributional patterns (Stiles compte & Jordano 2007), In the highly biodi- 1978, 1981). verse neotropics, more than 90% of tropical The purpose of this work was to study the plants depend on for seed dispersal structure of the mutualistic network of plants (Jordano 2000) and pollination (Bawa 1990). and hermit hummingbirds in the Colombian Hence these interactions are considered key Amazon, using like a model a hermit-plant drivers of biodiversity. community previously studied but from an Early studies of mutualistic interactions ecomorphological perspective (Rodríguez- between plants and animals focused on pair- Flores & Stiles 2005). Due to the tight cor- wise interactions (for a revision see Bascompte respondence among Hermits and , & Jordano 2007, Verdú & Valiente-Banuet we predict that the network will be: 1) highly 2008). With the development of modern heterogeneous because most hummingbird network analysis, recent studies view, explore species visits few plant species; 2) nested be- and analyze interactions by multiple species in cause specialists interact with subsets of the complex assemblages (Jordano 1987, Atmar & species in which generalists interact; 3) asym- Patterson 1993, Bascompte et al. 2003, Almei- metric with weak dependencies among species da-Neto et al. 2008, Verdú & Valiente-Banuet because few generalists provide most of the 2008, Jordano 2010), even from a geographi- services; and 4) some nodes inter- cal and evolutionary point of view (Dalsgaard act more strongly among them that with other et al. 2011). From these studies, networks of species of different nodes (Bascompte & Jor- plant- mutualisms tend to have diffuse dano 2007, Vázquez et al. 2009, Jordano 2010). and nested mutualistic interactions, where the interactions among different species (that METHODS can or can not share an evolutionary origin) are mostly facultative, of low specialization Study Area. Field work was done between No- and variable in time and space, with most of vember 2001 and July 2002 in the southern part connections concentrated in few core species of the Parque Nacional Natural Amacayacu (Jordano 1987; Bascompte & Jordano 2007, (PNNA) (Colombia, Amazonas; between 3°02’ Castaño Salazar 2009). and 3°47’S, 69°54’ and 70°25’W (Rudas 1996)) Hummingbirds (Aves: Trochilidae) live (Fig. 1). Mean annual temperature was 25.9°C, only in with more than 320 described and mean annual rainfall 3377 mm with one rainy species, mainly in the Neotropical region season (Amaya-Márquez 1991). In the study area (Stiles 1981). These feed on nectar and three vegetation types can be distinguished: riv- are pollinators of a large number of American erside, meadow and mainland (Amaya- Márquez

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FIG. 1. Location of Parque Nacional Natural Amacayacu, Amazonas, Colombia. Map courtesy of Parques Nacionales Naturales de Colombia (2011). et al. 2001). Field work concentrated in main- species were done in 8 hour periods (beginning land because this is the most extensive in at 5:30 h) for 10 out of the 20 days in each the area, and has the highest diversity of nectar visit. During the observation period we regis- resources for hermit hummingbirds (Cotton tered all the visits to the flowers, recording the 1998a). In mainland forest five sites were selected time, the hummingbird species that visited the and visited twice during study period for a total flowers, and the plant species visited by them. of 20 continuous days, separating visitation times Plant specimen was collected, identified and by at least 3 months among them. deposited in the Herbario Nacional Colom- and plant composition. To determine biano (COL) from the Instituto de Ciencias hermit hummingbird’s species and their nec- Naturales (ICN) of the Universidad Nacional tar resources, direct observation to focal plant de Colombia.

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Hummingbirds were captured using 5 mist original distribution of the data (Olesen et al. nets opened during 8 days per site from 06:00 2008). Statistical tests for distributions and to 12:00 h and from 14:00 to 17:00 h, alternat- AIC values were done using function brain- ing with observation days. Nets were placed in waver of R (R Development Core Team 2011). the same place where direct observations were Nestedness was calculated using two param- done, varying the placement of the nets be- eters (based on the qualitative matrix): Nested tween visits. From each captured hermit, pol- Temperature (NT, Atmar & Patterson 1993) len was obtained from bill, gorget and head and Nestedness metric based on Overlap and using a stained jelly to make a permanent slide Decreasing Filling (NODF, Almeida-Neto et al. for each individual (Amaya-Márquez 1991). 2008). Matrix temperature (Tº) is a measure of Pollen loads were analyzed in the Palynology disorder, where Tº50 means a perfect nested Laboratory of the ICN. matrix and Tº 5 100 a perfect not nested one Network structure. To study the structure of (Atmar & Patterson 1993). NT is defined as plant-hummingbird interactions, a quantitative NT 5 (100-Tº)/100 and varies between 0 and and qualitative matrix were constructed, with 1; matrix with NT 5 1 present a maximum hummingbirds placed in columns (H) and nestedness, NT 5 0.5 matrixes with random plants in rows (F). For the qualitative matrix, structure and NT 5 0 matrix with compart- rij 5 1 if the plant i was visited by the hum- ments (Bascompte et al. 2003). NODF has been mingbird j, and rij 5 0 if no interaction was proposed as a better parameter because: 1) it registered. For the quantitative matrix, the to- can calculate the nestedness between rows and tal number of visitations was recorded. To do columns independently, 2) allows the evalua- this, observations and pollen loads were taken tion of nestedness between one or more rows together assuming that: 1) For each pollen or columns with respect to others, and 3) is de- load, independently of the number of pollen pendent on the arrangement of columns and grains of each species on it, we assumed only rows, and so hypothesis can be tested regarding one visit of the hummingbird to each of these species order (Almeida-Neto et al. 2008). High species; 2) each time a hummingbird visited a values of NODF indicate that the matrix: 1) flower, independently of the number of flow- is high nestedness, 2) has a perfect 1’s overlap ers that the hummingbird visited in the same from right to left and from up to down, and bout, only one visit was counted. 3) has a decreasing marginal totals between all Using the information of the presence- pairs of columns and rows (Almeida-Neto et al. absence (qualitative) matrix, the cumulative 2008). To test the significance of the level of frequency distribution P(k) of the number of nestedness in the matrix, the values of Tº and interactions per node (k) was calculated. Prob- NODF were compared with two types of null ability was fitted to three different distribu- models: 1) ER: 1’s in the matrix were assigned tions: 1) exponential P(k) ; exp(-γk), 2) power randomly to different cells in the matrix, 2) CE: law P(k) ; k-γ, and 3) truncated power law the probability of having a 1 in the rij cell was

-γ  Pi Pj  P(k) ; k exp (-k/k ), where γ is a fixed con-  +  2 , where Pi is the number of presences x  C F  stant (degree of exponent) and kx is the trun- in the row i, Pj is the number of presences in cated value (Jordano et al. 2003, Bascompte the column j, C is the number of columns, and & Jordano 2007, Olesen et al. 2008, Castaño F is the number of rows (Guimarães & Gui- Salazar 2009). For each distribution, an Aikake marães 2006). This later model means that the information criterion (AIC) was calculated probability of having an interaction in the simu- considering that the distribution with the low- lated matrix is proportional to the generaliza- est value is the one that better represents the tion of plants and animals in the original matrix

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(Bascompte et al. 2003). 4000 random nets were and following this order the elimination of generated, 2000 for each model and inside that specific nodes was done; this procedure was 1000 were used to calculate mean Tº and the repeated 10 times. 2) Generalists to special- other 1000 mean NODF. Null models, Tº and ists: In this case we remove the species from NODF were calculated using ANHIDADO the more (i.e. generalists) to the less connected (Guimarães & Guimarães 2006). (i.e. specialist) nodes. 3) Specialist to gener- The asymmetry and evenness of the ma- alists: Here the less connected species were trix were calculated according to Vázquez et al. eliminated first, followed by the generalists. dij ∑ j (2009). Asymmetry index was defined as Ai = , After each simulation, we observed which spe- ki where ki was the number of species that in- cies left connected to the network, and one teracted with species i and dij is a measure of node was considered to be extinct when it lost the strength of the interaction between i and j all the interactions (Verdú & Valiente-Banuet (Vázquez et al. 2009). When one species has an 2008). asymmetry index close to 1 means that these af- A Binary Correspondence Analysis (ACB) fected strongly the species that interacted with was done using “VEGAN” package in R (R it but received low effects of the others; a value Development Core Team 2011). This proce- closet to -1 means that a species is influenced dure allowed us to detect association between strongly by others but has little influence over hummingbirds and plants based on similar re- them (Vázquez et al. 2007). Interaction evenness source use. The data used here was the visita- ij log* 2 pp ij index was defined as Shannon index H = tion frequency, calculated as the ratio between log 2F where pij is the proportion of interactions that the visits of one hummingbird species to a involved i and j, and F was calculated from in- plant species and the total number of visits of teractions observed in the matrix. An uneven this hummingbird species. This value is a good network (values closet to 1) is one with high measure of the intensity of plant use by hum- skewness in the 185 distribution of interaction mingbirds (Arizmendi 2001). frequencies (Vázquez et al. 2009). Parameters were calculated using functions “species level” RESULTS and “network level” of the bipartite package of R (R Development Core Team 2011). Seven hermits species were identified: Rufous- Resources’s Importance Valuation Index breasted Hermit ( hirsutus), Pale-tailed (IVIR, Amaya-Márquez et al. 2001), was used (Threnetes leucurus), Black-throated to determine the importance of each resource Hermit ( atrimentalis), Reddish Her- used by hermits in the community. For plants, mit (P. ruber), White-bearded Hermit (P. his- IVIR represents the rate between cumulated pidus), Straight-billed Hermit (P. bourcieri) and use intensities by hermit hummingbirds and Great-billed Hermit (P. malaris) (Remsen et al. number of hermit species. Higher IVIR values 2009). They visited 44 plant species with de- mean higher importance of the resource for tection by direct observations (8 plant species), hermits. palynological evidence (26 plant species), and To test the effect of hummingbirds and both methods (10 plant species). Families with plant species on the network, we highest number of visited species were Helico- simulated three different sequences of species niaceae (7 species), (7), Rubiace- : 1) Random: In this case, random ae (6), Acanthaceae (4) and Costaceae (3). The without replacement numbers were generated total number of matrix entries was 281 from for the number of plants (44) and humming- 407 direct observation hours and pallinogical birds (7) species that are forming the network, analysis of 50 slides (Table 1).

89 Rodríguez-Flores et al. 1 TOTAL PR Phaethornis ruber PA Phaethornis atrimentalis Threnetes leucurus Glaucis hirsuta Phaethornis bourcieri Phaethornis hispidus Phaethornis malaris Ca.al 0 0 0 0 0 0 1 1 Co.lon 1 0 0 0 0 0 0 1 Ga.cor 1 1 0 0 0 0 0 2 Ta.sip 1 0 1 0 0 0 0 2 Py.cup 1 0 1 0 0 0 0 2 Psy.pl 1 0 0 1 0 0 0 2 Psy.ba 0 0 0 1 1 0 0 2 Co.eri 1 1 0 0 0 0 0 2 Be.ex 1 1 0 0 0 0 0 2 Pas.co 1 0 1 0 0 0 0 2 Dr.ani 1 1 1 0 0 0 0 3 Psy.po 0 0 1 0 0 1 1 3 Ce.cor 1 1 1 0 0 0 0 3 Sa.per 1 1 0 1 1 0 0 4 Pa.las 1 1 0 1 1 0 0 4 Dr.coc 1 1 1 0 1 0 0 4 Be.ag 1 1 1 0 0 0 1 4 He.sta 1 1 0 1 1 0 0 4 He.aff 1 1 0 1 1 0 0 4 Gu.spi 1 1 1 0 0 1 0 4 He.str 1 1 1 1 1 0 0 5 Dr.sem 1 1 1 1 1 0 0 5 Co.sca 1 1 1 1 0 0 1 5 Du.hir 1 1 1 1 1 0 0 5 Abrev. PM PH PB GH TL Calathea altissima Costus longebractulatus Gasteranthus corallinus Tabernaemontana siphilita Tabernaemontana Psittacanthus cupulifer platypoda Psychotria Psychotria bahiensis Psychotria Columnea ericae Bertholetia excelsa coccinea Passiflora Drymonia anisophylla Psychotria Centropogon cornutus Sanchezia peruviana lasiantha Palicourea Drymonia coccinea aggregata Heliconia standleyi Heliconia aff.standleyi Gurania spinulosa Heliconia stricta Drymonia semicordata Costus scaber Duroia hirsuta Marantaceae Costaceae Gesneriaceae Apocynaceae Loranthaceae Rubiaceae Gesneriaceae Lecythidaceae Passifloraceae Gesneriaceae Rubiaceae Campanulaceae Acantaceae Rubiaceae Gesneriaceae Gesneriaceae Heliconiaceae Heliconiaceae Cucurbitaceae Heliconiaceae Gesneriaceae Costaceae Rubiaceae TABLE 1. Interaction matrix ofInteraction 1. TABLE hermit Thein PNNA. resources nectar hummingbirds and their representinteractions getdata the observadirect during the - ofpresence 1= and pollen loads. tions of 0=lack interaction, The interaction. are arrangedspecies nestedness. for maximum criteria NODF the according to line includes the most generalist species. The the black area enclosed by FAMILY SPECIES 90 HERMIT HUMMINGBIRD-FLOWER POLLINATION NETWORK 1 TOTAL 0 1 PR Phaethornis ruber 1 PA Phaethornis atrimentalis Threnetes leucurus Glaucis hirsuta Phaethornis bourcieri Phaethornis hispidus 000 01 11 1 01 0 00 01 0 01 0 0 00 0 00 0 0 01 0 0 0 0 11 0 0 0 1 0 01 0 0 0 0 00 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 0 0 0 0 1 0 1 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 1 0 0 0 0 0 1 0 0 0 1 0 1 0 0 1 0 1 0 1 0 1 0 1 1 1 31 19 14 11 10 6 4 95 Phaethornis malaris 2 Di.uc 0 0 0 0 0 1 0 1 Ta.het Co.lle Psy.bl Dr.ser Me.lin Er.fusHe.hir Is.pub 1He.jul Pas.vi Co.ery Cu.me 0He.jur He.spa 0Ru.cha Ps.gui 0Pseu.TOTAL 0 0 0 0 0 0 1 0 1 0 0 1 Sa.put 1 0 0 0 0 0 0 1 Abrev. PMCa.con PH 0 PB 0 GH TL 0 0 0 Dioclea ucayalina Tabernaemontana Tabernaemontana heterophylla Combretum llewelynii Psychotria blephanophora Drymonia serrulata Mendocia lindavii Erythrina fusca Heliconia hirsuta Ischnosiphon puberulus Heliconia julianii vitifolia Passsiflora Costus erythrocoryne Cuphea melvilla Heliconia juruana Heliconia spathocircinata Ruellia chartacea Psidium guineense Pseudobombax sp. Sanchezia putumayensis Calathea contrafenestra Number of plant species. total records for each Number of hummingbird species. total records for each Fabaceae TABLE 1 (Continuation). TABLE FAMILY SPECIES Marantaceae Apocynaceae Combretaceae Rubiaceae Gesneriaceae Acantaceae Fabaceae Heliconiaceae Marantaceae Heliconiaceae Passifloraceae Costaceae Lytraceae Heliconiaceae Heliconiaceae Acantaceae Myrtaceae Acantaceae Malvaceae 1 2

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The cumulative frequency distribution of random structure (NODF 5 47.64) but sig- the network (P (k)) was heterogeneous. 90% nificantly nested with respect to null models of the total species forming the network had (NODF ER model 5 33.18, p , 0.01; NODF 6 or less connections (all plants and two her- CE model 5 38.26, p , 0.01). mits), while 5 species (all hermits) were more The network was highly uneven (H = 0.90) connected than expected by chance (hav- and asymmetrical (Fig. 3), indicating that the ing between 10 and 31 connections) (Fig. 2; number and intensity of connections among Bascompte & Jordano 2007, Castaño Salazar species were not homogeneous. The seven 2009). This network had a better fit to power hermit species affected importantly the 44 law (γ 5 2.22) than to exponential (γ 5 0.27) plant species used by them (values of A › 0), or truncated power law functions (γ 5 1.15, while the plants had no significant effect over k 5 3.24; Fig. 2). x hummingbirds (Ai ‹ 0) (Fig. 3). The network analyzed here was nested, Hermits and the plant species that they vis- with the level of nestedness variable accord- ited formed a highly cohesive network, with a ing to the different parameters reviewed. The core group of generalist’s hummingbirds that NT value indicated that this network was high- visited both generalist and specialist plants ly nested ( Tº 5 23.75, NT = 0.76) and sig- (Fig. 4). Most of the interactions were classi- nificantly different from random matrixes (Tº fied as weak (less than 5% of the plants had model ER 5 61.65, p . 0.01; Tº model CE 5 46.62, p , 0.01). The NODF value showed a

FIG. 2. Cumulative frequency distribution (P (k)) of the number of links (k) for a hermit humming- bird-plant mutualistic network in the Colombian Amazon. The graph in a log-log scale combine as plant as hummingbird interactions. The original data (circles) was adjusted to three distributions: 1) power-law function (pot.), 2) exponential (exp.) and FIG. 3. Asymmetry Index (Ai) of the seven her- 3) truncated power-law (pot.trun.). This network mit hummingbird species (top) and 44 plant species 5 has a better fit to the power-law function (AICexp. (bottom) visited by them in PNNA. For species’ ab- 5 5 238.150, AIC pot. 167.659, AIC pot.trun. 237.546). breviations see Table 1.

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work changed according elimination order (Fig. 5). This network was more sensitive to the elimination of generalist than of special- ist species, while random elimination had an intermediate effect on the number of spe- cies that remained connected to the network. The network resisted better the elimination of plants than of hummingbirds, because all hummingbird species remained attached to the network after losing 50% of the plants inde- pendently of the order of elimination (Fig. 5). ACB explained 74% of data variance and divided the community in three associations (Fig. 6): 1. First association (Fig. 6A) was composed by the Black-throated Hermit and four plant species visited only by them. The flowers of this plants look like ento- mophilous species (Faegri & van der Pijl 1979) having short to medium corollas (22.66 6 12.56 mm; Rodríguez-Flores & FIG. 4. of hermit humming- Stiles 2005). birds (black boxes) and plants (grey boxes) on the 2. Second association (Fig. 6A) was formed Colombian Amazon. The lines represent the 95 in- by , Straight-billed Her- teractions registered, and the box size is proportion- mit and seven plant species. The four al to the number of species with which each species species visited by Reddish Hermit be- is interacting. For species’ abbreviations see Table 1. longed to this association, and three of them (with exception of Calathea IVIR › 0.1), while trophic dependence was altissima) were also visited by two more different for each guild: 50% of plant species hermit species. Of the 14 plant species were highly dependent on one or two hum- used by the Straight-billed Hermit, the mingbird species, while 5 out of the 7 hermit five more intensively visited, belonged species used 10 or more plant species as nectar to this association. Flower morphologies resources. Some species represented key nodes and growth form of these species were because they connected specialized species to very different, including vines, herbs the network (Castaño Salazar 2009). These key and trees, and flowers with red, orange, species were the Great-billed Hermit and the yellow and white corollas (Rodríguez- White-bearded Hermit. Great-billed Hermit Flores & Stiles 2005). was the main visitor of 15 plant species, 10 of 3. Third association (Fig. 6B) was formed which were visited exclusively by them; White- by the heavier four hummingbird spe- bearded Hermit visited 9 plant species, three cies (Great-billed Hermit, White-beard- of which were only visited by them (Appendix ed Hermit, Rufous-breasted Humming- 1, Fig. 4). bird and Pale-tailed Barbthroat and 33 The number of hummingbirds and plants plant species (see Rodríguez-Flores & species that remained connected to the net- Stiles 2005 for morphological informa-

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FIG. 5. Percentage of plants (A) and hummingbirds (B) that remain connected to the network after coex- tinction simulations following three scenarios: generalist first, specialist first and random elimination (each point represents the mean value, and the line the standard deviation)

FIG. 6. Binary Correspondence Analysis for the seven hermit hummingbird species (gray points) and the 44 plant species (black points) visited by them in the PNNA. The numbers 1, 2 and 3 in the top figure (A) represent the principal associations formed by the analysis; B figure is a close up of the group 3 (see text for details). Species’ abbreviations in Table 1.

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tion). In this group is relevant: 1) The Fork-tailed Woodnymph (Thalurania furcata), a location close to the origin of the ordi- resident and abundant species in the study area nation on the graph, and 2) the overlap (Cotton 1998a). A possible network taking between plant specie’s positions on the into consideration both groups of humming- graph, indicating that many of the plant birds should show a clear separation between shared their flower visitors. and Phaethornithinae interactions. Also, a complete year-round study may prob- DISCUSSION ably not add any hermit hummingbird to the network nor find huge changes in humming- The community analyzed here can be de- bird’s abundances according to what is found scribed as a diverse guild of hermit humming- by other studies (e.g. Cotton 1998ab, Amaya- birds (7 species, Cotton 1998a) and plants vis- Márquez et al 2001). With this in mind, is pos- ited by them (44 species; Rodríguez-Flores & sible that when include more time, new plant Stiles 2005). Hermits used resources with mor- species could be added to the network, acting phologies not typically classified as humming- like specialist nodes that will make the network bird species (less than 70% of the plant species more nested and cohesive (Bascompte & Jor- being classified as ornitophylous; Rodríguez- dano 2007). Flores & Stiles 2005). However, bigger species The fit of the cumulative frequency distri- tended to use more ornitophylous species (ac- bution to the power law function, imply that cording to Faegri & van der Pijl 1979). This this network follow a preferential attachment pattern has been found elsewhere (i.e. Amaya- mechanisms (Bascompte & Jordano 2007), in Márquez et al. 2001), suggesting that in spite of other words, this means that in evolutionary the opportunistic behavior of hummingbirds, time, generalist species become more general- among Hermits selective pressures have main- ists because (by probability) new nodes tend to tained fidelity with ornitophylous flowers as interact preferentially with the most-connected those of the genus Heliconia (Stiles 1978, 1981). nodes (Vázquez & Aizen 2003, Bascompte & Mutualistic network analyzed here was Jordano 2007). Nestedness in ecological nets incomplete due mainly to 1) temporal incom- arises when generalist interacting with other pleteness (only 9 months surveyed) and 2) the generalist, specialist interact with a particular lack of all the Trochilinae members. Howev- subset of generalist, and interactions between er, the months included are the most diverse specialist are very rare (Bascompte et al. 2003, both in flowering plants as hummingbirds in Verdú & Valiente-Banuet. 2008). Plant-hum- the studied site (41 species flowering from mingbird mutualistic networks are specialized November to July, 14 species from August to (Dalsgaard et al. 2012), just like the network an- October; Cotton 1998b), and Trochilinae are alyzed here, however the NT value was lower more abundant in forest canopy and secondary than those found for other pollination (NT 5 vegetation (Cotton 1998b, Rodríguez-Flores & 0.85 6 0.05), dispersion (NT 5 0.84 6 0.04) Stiles 2005). This spatial segregation between and facilitation (NT 5 0.89 6 0.03) networks the two subfamilies had implications in the (Bascompte et al. 2003, Verdú & Valiente-Ban- low overlap in resource use by the two groups uet. 2008, Castaño Salazar 2009). The NODF (Amaya-Márquez et al 2001). Moreover, dur- parameter got (NODF 5 47.64) indicated ing observation bouts no Trochilinae species that the net had a random structure but more was registered visiting flowers, and only 13.6% nested than other positive interaction net- of the total net captures corresponded to this works (NODF 5 26, Verdú & Valiente-Banuet subfamily with only one registered species, the 2011). This reflects the fact that the plants in

95 Rodríguez-Flores et al. the network (in opposition to the humming- nected to the network by convergence, because birds) broke the decreasing fill condition of hermits represent a monophyletic group in Tro- the index (Table 1) (Almeida-Neto et al. 2008). chilidae (McGuire et al. 2009), and where the spe- In other words, this means that the humming- cialized diet had resulted in a common general birds were responsible of the nested structure structure, with particular morphological, physi- observed, because the generalist hermits in- ological and behavioral adaptations (Brown & corporated generalist and specialist plant spe- Bowers 1985, Rosero 2003). In other side, plants cies to the network and concentrated the most visited by hermits belonged to diverse phyloge- part of the links, whereas the specialist hermits netic groups, with basal groups represented by connected to the generalist plant species. (genus Heliconia, Calathea, Costus) One of the principal hypothesis proposed and terminal groups by Asterales species (genus to explain causes of nestedness on ecological Centropogon) (Stevens 2001). Probably plant spe- networks is the abundance of the species (Le- cies had been connected to the net by conver- winsohn et al. 2006), and the more connected gence/complementarily. Interactions between hermit species in this network (the Great-billed hermits and Heliconia plants in the community are Hermit and the White-bearded Hermit) were a good example of complementarily, mainly in the more captured in the mist-nets (76% of all the co adaptation shown by bills and corollas that captured hummingbirds) and also the more ob- results in a high pollination specialization (Stiles served species (39.83%). For the plants the rela- 1975, Temeles & Kress 2003). Convergence is tion was not so clear, because most of them were not so easily shown in the community. However, only connected with one hummingbird species the presence of resources as Psidium guineense or and their abundance was not related to number Tabernaemontana heterophylla that have flowers not of connections (Rodríguez Flores 2004). adapted for hummingbird visitation, suggest that A second explanation for nestedness in mu- these hummingbirds are generalist and could tualistic networks is the phenotypic convergence be selecting other traits different to length and and complementarily between groups (Santama- corolla’s curvature. The connection of these re- ría & Rodríguez-Gironés 2007). Complemen- sources to the net through the visitation of key tarily has been defined as the functional match hummingbird species, can lead to evolution of between phenotypic traits in the interacting spe- convergent traits in those plants (Thompson cies, traits that can directly affect the reproductive 2010). success of the species connected. Once the pair- Interactions between hummingbirds and wise interaction is established, other species can plants were asymmetrical and weak, with the be added to the network by convergence to these importance (measured like the dependence traits (Bascompte & Jordano 2007, Rezende et between species) concentrated among hum- al. 2007). In the context of hummingbird-plant mingbirds whose formed a core node to which interaction, has been established that the mor- other species can join the net (Jordano 2010) phological traits that are determining the food (Fig. 3). This showed that in spite of all mor- patterns, diversity and specificity between these phological and behavioral restrictions, these birds and their nectar resources are weight, beak’s hermit hummingbirds behave as generalist length and curvature, and corolla’s length and visiting a high diversity of resources (Buzato curvature (Stiles 1981, 1995, Kodric-Brown et 1995, Cotton 1998b, Gutierrez & Rojas 2001, al. 1984, Brown & Bowers 1985, Cotton 1998b, Rosero 2003, Borges & Machado de Almei- Gutierrez & Rojas 2001, Rosero 2003, Temeles da 2011, Gómez & Quintana 2011). For the & Kress 2003, Rodríguez-Flores & Stiles 2005). plants we found very contrasting examples. In our case, no hummingbird species were con- Passsiflora vitifolia depended almost completely

96 HERMIT HUMMINGBIRD-FLOWER POLLINATION NETWORK on the Great-billed Hermit for its connection fragile to the extinction of generalist species (Al- to the net, but for these hummingbird P. vitifo- bert et al. 2000, Bascompte & Jordano 2007). The lia was a low importance resource used in low study of complex networks has the ability of pre- intensity (IVIR 5 0,002). The other extreme, dicting the possible outcomes of species extinc- was Costus scaber, a generalist plant species vis- tions on the structure and functionality of the ited by 5 hummingbird species, but used very network (Srinivasan et al. 2007). The extinction intensively for a specialist hummingbird spe- simulations highlight the importance of general- cies, the Reddish Hermit (Appendix 1, Fig. 3). ist hummingbirds as core species in the structure Like other mutualistic networks, the one of this mutualistic network (Fig. 5A). Same results studied here was formed by multiple modules were found in another study regarding bats and that act as the basic blocks of the network (Bas- dispersed plants, where plants were highly fragile compte & Jordano 2007, Jordano 2010; Fig. to the elimination of a few generalist bats (Casta- 4). Species inside these modules interact more ño Salazar 2009). However, in difference to the strongly among them than with others (Fig. 4), facilitation network studied by Verdú & Valiente- and groups were joined by generalist species Banuet (2008), in our network was impossible to as the Rufous-breasted Hermit and the Great- assume that the species of one group are strongly billed Hermit through non specific interactions dependent of the species in the other to survive (Bascompte & Jordano 2007). In ecological nets and that such dependence is species specific, there are some restrictions, (morphological and/ because we did not take into account the other or phonological) that make impossible some non-hummingbirds pollinators, and did not have connections (Bascompte & Jordano 2007). This information about hummingbird’s pollination ef- concept of “forbidden links” has been used to ficiency. If we take into account the generalist be- explain the structure in ecological networks in havior of the hummingbirds, is highly probable opposition to the neutral models where pheno- that if we eliminate one hummingbird species, typic traits of interacting species are considered and by consequence some plant species lost their irrelevant (Bascompte & Jordano 2007, San- connections to the network, another hermit will tamaría & Rodríguez-Gironés 2007). Phenotypic use the flowers that the previous species visited, coupling in hummingbird-plant systems, and the opening the possibility that these species to be importance of the morphological traits on this reconnected to the network. Furthermore, facing process has been described previously (Stiles this network to a random extinction process, we 1975, Gutierrez & Rojas 2001). Forbidden links would predict that this will remain stable even if can be the more reasonably explanation to many we remove an important number of nodes, this of the non-observed interactions. The Reddish because the most part of the species are special- Hermit (exposed culmen 5 23.38 6 0.60 mm) ist (in our case principally plant species) and the for example, did not visited flowers of Heliconia probability of remove a generalist node from the stricta (total corolla 5 68.35mm) in spite of being network is low (Castaño Salazar 2009). However, present at the same time and at the same place although nested networks are robust to species (Rodríguez-Flores & Stiles 2005). loss, this tolerance has a limit before the collapse Network architecture (measure as its hetero- (Bascompte & Jordano 2007), and with the simu- geneity and nestedness) can have huge implica- lation of the species extinction like we used here, tions in the robustness of the network, in other we can have an idea of the network tolerance. words, its ability to resist species loss (Bascompte We could illustrated that a community approx- & Jordano 2007). When a network fitted better imation to the hummingbird-plant interaction, to the power law function (like the one studied that goes forward the traditional pairwise perspec- here) is resistant to random losses of species, but tive, gives new perspectives about the mechanisms

97 Rodríguez-Flores et al. that organize and structure the ecological com- Almeida-Neto, M., P. Guimarães, P. R. Guimarães, munities. At the same time, this approximation R. D. Loyola, & W. Ulrich. 2008. A consistent opens news and interesting possibilities to move metric for nestedness analysis in ecological a step forward and study the ecological communi- systems: reconciling concept and measurement. ties in terms of the species’ evolutionary history Oikos 117: 1227–1239. and of the effect that can have the extinction of Amaya-Márquez, M. 1991. Análisis palinológico de the species and the interactions in the conserva- la flora del Parque Nacional Natural Amacayacu tion and the preservation of the ecosystems. For (Amazonas) visitada por colibríes (Aves: future studies it is necessary to include informa- Trochilidae). Grad. thesis, Univ. Nacional de tion about contemporary and historical climate, Colombia, Bogota, Colombia. temporal and spatial variability and their effect on Amaya-Márquez, M., F. G. Stiles, & O. Rangel. the network structure, factors that are also relevant 2001. Interacción planta-colibrí en Amacayacu to understand the processes that are driving and (Amazonas, Colombia): una perspectiva structuring biotic specializations (Vázquez et al. palinológica. Caldasia 23: 301–322. 2009, Dalsgaard et al. 2012). Arizmendi, M. C. 2001. Multiple ecological interactions: nectar robbers and hummingbirds in a highland ACKNOWLEDGMENTS forest in . Can. J. Zool. 79: 997–1006. Arizmendi, M. C. & C. Rodríguez-Flores. 2012. We want to acknowledge to the Unidad Admin- How many plant species do hummingbirds istrativa Especial Del Sistema de Parques Na- visit? Orn. Neotrop (Present number). cionales de Colombia (UAESPNN) and to the Atmar, W., & B. Patterson. 1993. The measure of personal of the PNNA, especially to S. Bennett order and disorder in the distribution of species and A. Parente, for their constant support. To in fragmented . Oecologia 96: 373–382. Foundation Tropenbos Colombia and IDE- Bascompte, J., & P. Jordano. 2007. Plant-Animal AWILD for financial support. To the bird col- Mutualistic Networks: The Architecture of lection, palinological laboratory and National Biodiversity. Ann. Rev. Ecol. Evol. Syst. 38: Herbarium of Colombia (COL) from the In- 567–593. stituto de Ciencias Naturales de la Universidad Bascompte, J., P. Jordano, C. J. Melián, & J. M. Nacional de Colombia, for logistic support. We Olesen. 2003. The nested assembly of plant– thank S. Wethington and C. Lara for revision of animal mutualistic networks. PNAS 100: 9383– the manuscript, and P. Guimarães for some ad- 9387. vices about the methods. H. Castaño, M. Amaya Bawa, K. 1990. Plant-pollinator interactions in and P. Cotton for their information. G. Bogotá tropical rain forests. Annu. Rev. Ecol. Syst. 21: worked in the identification of some of the pal- 399–422. ynomorphs. We thank S. Suarez, J. Betancur and Borges, S. H., & R. A. Machado de Almeida. 2011. M. Amaya for the identification of some plants. Birds of the Jaú National Park and adjacent CONACyT fellowship 46248 to CIRF and Pos- areas, Brazilian Amazon: new species records grado en Ciencias Biológicas UNAM allowed with reanalysis of a previous checklist. Revista the analysis and writing of this paper. Brasileira de Ornitologia 19: 108–133. Brown, J. H., & M. A. Bowers. 1985. Community REFERENCES Organization in Hummingbirds: Relationships between Morphology and Ecology. Auk 102: Albert R, H. Jeong, & A L. Barabasi. 2000. Error 251–269. and attack tolerance of complex networks. Buzato, S. 1995. Estudo comparativo de flores Nature 406: 378–82. polinizadas por beija-flores em tres comunidades

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