Temporal Variation in Pollination Services to Cucurbita Moschata Is
Temporal variation in pollination services to Cucurbita moschata is determined by bee gender and diversity 1,2,3 1 1,4 1,4 OLIVERIO DELGADO-CARRILLO, SILVANA MARTEN-RODRIGUEZ, LORENA ASHWORTH, RAMIRO AGUILAR, 1,5 1,2, MARTHA LOPEZARAIZA-MIKEL, AND MAURICIO QUESADA
1Laboratorio Nacional de Analisis y Sıntesis Ecologica (LANASE), Escuela Nacional de Estudios Superiores Unidad Morelia, Universidad Nacional Autonoma de Mexico, Morelia, Michoacan 58190 Mexico 2Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autonoma de Mexico, Apartado Postal 27-3, Morelia, Michoacan 58089 Mexico 3Instituto de Ecologıa, Universidad Nacional Autonoma de Mexico, Mexico, D.F. 04510 Mexico 4Instituto Multidisciplinario de Biologıa Vegetal, Universidad Nacional de Cordoba – CONICET, Cordoba 5000 Argentina 5Facultad de Desarrollo Sustentable, Universidad Autonoma de Guerrero, Tecpan de Galeana, Guerrero 40900 Mexico
Citation: Delgado-Carrillo, O., S. Mart en-Rodr ıguez, L. Ashworth, R. Aguilar, M. Lopezaraiza-Mikel, and M. Quesada. 2018. Temporal variation in pollination services to Cucurbita moschata is determined by bee gender and diversity. Ecosphere 9(11):e02506. 10.1002/ecs2.2506
Abstract. It has been proposed that species-rich insect communities and species turnover across land- scapes enhance the pollination efficiency of crops through complementarity, where both the dominant and less abundant species contribute to reaching a yield threshold from pollination. Alternatively, fluctuations in the most abundant pollinator species, rather than changes in species richness, may drive temporal varia- tion in pollination services. In this study, we used Cucurbita moschata as a model to investigate temporal variation in pollinator communities in a Mexican tropical dry forest region. We sampled floral visitors in the coastal region of Jalisco during the wet and dry seasons and determined the pollination efficiency of all floral visitors. Our results showed that there was temporal variation in the pollinator community and in the pollination efficiency of the main pollinators of Cucurbita moschata crops. In the wet season, native bees of the genus Peponapis were the most frequent and effective pollinators of C. moschata, whereas in the dry season, Peponapis bees were scarce and Apis mellifera became the most frequent floral visitor. Apis mellifera transfers smaller pollen loads than Peponapis, but it provides an effective pollination service in conjunction with other native bees during the dry season. There was also an interaction between flower gender and pollinator species, where A. mellifera had higher visitation rate to female C. moschata flowers, and Peponapis bees to staminate flowers. Mean visitation rate by Peponapis female bees was 17 times higher than visitation rate by male bees. This is the first report of a vis-a-vis relationship of pollinator gender with respect to plant gender in which plants of the genus Cucurbita that produce unisexual staminate and pistillate flowers are differentially visited by Peponapis male and female bees, where females are the main pollinators. Under- standing the temporal variation in pollinator communities and the contribution of the different species of pollinators to the reproductive success of different crop species and varieties can be crucial to maintaining pollination services under the current global pollination crisis.
Key words: Apis mellifera; bees; crop pollination; fruit set; native pollinators; Peponapis; plant reproductive success; pollination service; pollinator gender; seed production; squash; tropical dry forest.
Received 30 September 2018; accepted 9 October 2018. Corresponding Editor: Debra P. C. Peters. Copyright: © 2018 The Authors. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail: [email protected]
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INTRODUCTION Temporal variation in pollinator services in tropical regions is relevant to annual and peren- Recent evidence of the decline of introduced nial crops with long or inducible flowering sea- and wild pollinators in North America and Eur- sons. Most crop species are annual and have a ope has caused great concern worldwide given single flowering season per year. However, irri- its potentially catastrophic consequences on food gation allows cultivation at different times of the security (Potts et al. 2010a, b). The global decline year, enabling farmers to harvest more than once in pollinator abundance has caused a reduction a year, especially in areas near rivers and wet- in pollination services and crop yields (Millen- lands (Armillas 1949). This is the case of crops nium Ecosystem Assessment 2005). Under this that are cultivated in Neotropical dry forest scenario, the conservation of native pollinators regions during the dry and wet seasons, such as may be crucial to ensure crop pollination success the squash, Cucurbita moschata. Given that plant (Winfree et al. 2007, Garibaldi et al. 2013), since flowering time and pollinator activity should be the contribution of native pollinators to fruit and evolutionarily tuned to maximize both plant and seed production is often higher than the contri- pollinator fitness, native pollinators should be bution of introduced pollinators (Canto-Aguilar present or active during the natural flowering and Parra-Tabla 2000, Gibbs et al. 2016). This is season of a native crop species. Moreover, the possibly the result of a shared evolutionary his- native pollinators of a crop species should be tory between plants and native pollinators that more effective than introduced pollinators. How- has often resulted in specialized plant–pollinator ever, if native pollinators are absent when native interactions (Ashworth et al. 2009, Gibbs et al. crops are cultivated out of their season, then 2016). Studies investigating pollination services introduced pollinators may provide alternative of native pollinators to crop species are increas- pollination services. ingly important to ensure global food security, In agricultural fields of the tropical dry forest crop productivity, and yield stability. regions of Mesoamerica, farmers take advantage Despite the importance of native pollinators for of natural rainwater in the wet season to grow crop productivity, only a few studies have docu- crops like maize, backyard squash (Cucurbita mented the performance of native pollinator spe- moschata) and crops for livestock food. Crops of cies and the impact of seasonal changes of the C. moschata are mainly cultivated for self-con- pollinator community on crop productivity. sumption. In the dry season, agriculture is more Diverse pollinator communities provide more technified because farmers need to irrigate their stable and efficient pollination services (Hoehn crops from nearby water sources. Farmers gener- et al. 2008, Klein et al. 2009, Rogers et al. 2014, ally use the alluvial soils of riverbanks that flood Winfree et al. 2018), and temporal changes of pol- during the wet season but remain arable land dur- linator assemblages through the year may con- ing the dry season. This practice eliminates the risk tribute to the diversity of pollinator communities of flooding and loss of crops that often occurs in and to the stability of crop production. Alterna- the wet season. Furthermore, because the popula- tively, seasonal variation in primary pollinators or tions of many adult insect herbivores are reduced the lack of efficient pollinators in one season may during the dry season, there should be lower her- result in a seasonal reduction in crop production. bivory (Dirzo and Dom ınguez 2002, Cuevas-Reyes Temporal changes in pollinators have been docu- et al. 2006), which is expected to increase crop mented for Citrullus lanatus and Vaccinium angusti- yields.InMexico,somecropsaregrowninboth folium in North America (Kremen et al. 2002, the dry and wet seasons, and include various spe- Bushmann and Drummond 2015); however, little cies of squashes, such as C. moschata and C. pepo. is known about temporal variation in pollinator These species are ideal to evaluate temporal and communities and pollinator efficiency in tropical spatial variation in pollinator assemblages and regions. To propose viable strategies for the man- pollination services for native crop species. agement and conservation of pollinator services The genus Cucurbita is a group of monoecious, for tropical crops, it is necessary to understand self-compatible plants, pollinated mainly by how changes in pollinator communities impact bees, and cultivated worldwide (Hurd et al. crop production across different seasons. 1971, Lira-Saade 1995). There are about 27
❖ www.esajournals.org 2 November 2018 ❖ Volume 9(11) ❖ Article e02506 DELGADO-CARRILLO ET AL. species, of which five species have been domesti- of plants occurs within one to three months, and cated: C. pepo, C. ficifolia, C. moschata, C. maxima, flowering lasts approximately two to three and C. argyrosperma (Whitaker 1974, Lira-Saade months (Lira-Saade and Montes 1992). Cucurbita 1995). Mexico is considered an important center moschata has staminate and pistillate yellow- of genetic diversity of the genus Cucurbita (Lira- orange flowers on the same individual plant. Saade and Montes 1992, Lira-Saade 1995); since Floral anthesis lasts approximately six hours, pre-Hispanic times, four of the five species have with flowers opening just before dawn and been domesticated in the country, and 11 wild- closing at noon. Both types of flowers produce type taxa have been recorded (Lira-Saade 1995). abundant nectar. Staminate flowers have a long Bees of the genus Peponapis have been docu- pedicel, measuring between 16 and 18 cm. Pistil- mented as the main pollinators of Cucurbita late flowers have shorter pedicels, 3–8 cm long, (Hurd et al. 1971, 1974, Tepedino 1981, Canto- three-lobed stigmas, and an ovary that contains Aguilar and Parra-Tabla 2000), although some approximately 700 ovules (Canto-Aguilar and studies report other bee genera as frequent floral Parra-Tabla 2000). The pollen grains are large visitors (Artz et al. 2011, Enr ıquez et al. 2015). and sticky; thus, their transfer requires a biotic Peponapis is exclusive to the American continent, vector (Free 1993). Pollinators of C. moschata are and in particular, Peponapis pruinosa and P. crassi- essential for fruit and seed production (Klein dentata share a close evolutionary history with et al. 2007). the distribution and domestication of Cucurbita (Lopez-Uribe et al. 2016). Study site We evaluated the pollination services to Cucur- We conducted the study in the municipalities bita moschata in the coastal region of Jalisco, Mex- of Cihuatlan and La Huerta, located in the south- ico, during the wet and dry seasons. Cucurbita west coast of Jalisco, Mexico. The altitude in this moschata is an ideal study species because it is region ranges from 0 to 1300 m.a.s.l. The climate highly dependent on pollinators for seed produc- is predominantly warm subhumid with summer tion (Free 1993, Klein et al. 2007); in North Amer- rains, with a mean annual temperature of 20– ica, native and introduced bees perform most of 28°C, and a mean annual precipitation of 600– the pollination (Tepedino 1981, Canto-Aguilar 2000 mm. Agriculture occupies 21–25% of the and Parra-Tabla 2000, Artz et al. 2011), and in area of the municipalities (INEGI 2009), while tropical dry forest habitats, crops are cultivated tropical dry forest occupies 56.1% of the coastal during both dry and rainy seasons. We studied area of Jalisco (Sanchez-Azofeifa et al. 2009). the pollinator community composition, foraging Crops of Cucurbita moschata are cultivated dur- behavior, and efficiency of pollinators for fruit ing the wet and the dry seasons. The dry season and seed production of C. moschata across two in this tropical dry forest begins in November seasons. Peponapis and Xenoglossa bee species are and lasts to the end of May. This season coincides pollen specialists on Cucurbita, and have active with the cultivation of other pollinator-depen- nests during the wet season, coinciding with the dent crops such as watermelon (Citrullus lanatus), natural flowering time of Cucurbita (Rozen and tomatillo (Physalis ixocarpa), chili (Capsicum Ayala 1987, Ayala 2004, Delgado-Carrillo et al. annuum), cucumber (Cucumis sativus), chayote 2017). Therefore, we predict that during the wet (Sechium edule), and tomato (Solanum lycoper- season, the pollinator community of C. moschata sicum). The wet season begins in June and lasts crops will be dominated mainly by native bees until October–November. Cultivation of other with high pollination efficiency. In the dry sea- pollinator-dependent crops (e.g., tomatillo, Phy- son, the pollinator community should change to salis ixocarpa; and watermelon, Citrullus lanatus) more generalized and less efficient pollinators. in this season is rare because farmers avoid culti- vating these crops to prevent the risk of losing MATERIALS AND METHODS crop production to flooding or pests. We con- ducted our sampling at five Cucurbita moschata Study plant cultivated fields, two field plots during the wet Cucurbita moschata is an annual herbaceous, season of 2015 (mid-September–October) and climbing, and monoecious plant. Full development three field plots during the dry season of 2016
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(January–March). Specific coordinate locations visitors, 3–15 individuals of each species) and are provided in the supplementary material examined pollen loads. Captures were performed (Appendix S1: Fig. S1). between 8:00 and 10:00 hours. Each individual was captured on a separate killing vial. We Pollination community and foraging behavior removed pollen from each animal body dabbing We evaluated differences in the composition of one piece of fuchsin gel over four different parts the pollinator community and in visitation pat- of the pollinator body, maintaining the samples terns between seasons, flower genders, and polli- separated: back, head, ventral abdomen, and nator species. We conducted 190 h of video ventral torso. We did not remove pollen from spe- recording, focusing on staminate and pistillate cialized structures for pollen transport (i.e., corbic- flowers from 7:00 to 11:30 hour, in both the dry ulae, scopae). We deposited each pollen sample and the wet seasons. In the wet season, we filmed on a slide, and counted the number of pollen 10 staminate flowers and ten pistillate flowers on grains of C. moschata with a stereoscopic micro- 20 individual plants (i.e., one flower observed per scope and the Zen program V 1.1.2 (Zen 2012). plant) in two different plots, plot one with 8 flow- For statistical analyses of pollen samples, we con- ers and plot two with 12 flowers (Appendix S1: sidered Peponapis crassidentata and P. utahensis as Fig. S1). In the dry season, we filmed 15 staminate a single taxon to be consistent with other analyses flowers and 17 pistillate flowers on 32 individual because we could not discriminate among these plants (i.e., one flower observed per plant) in species on video recordings. We analyzed pollen three different plots, plot three with 13 flowers, loads separately for male and female Peponapis plot four with 9 flowers, and plot five with 10 because they visit flowers at different rates and flowers (Appendix S1: Fig S1). For each floral carry different amounts of pollen. visit, we recorded the pollinator species (to the lowest possible taxonomic level), time of arrival at Pollinator efficiency experiments the flower, and duration of the visit; we also To evaluate pollinator efficiency and the relative quantified pollination events by registering visi- contribution of the different species to the pollina- tors’ contact with the reproductive organs of the tion of C. moschata, we performed exclusion flower. For identification, we collected individuals experiments at the five field plots during the flow- of each floral visitor species and used the bee spe- ering season of the crop. These experiments were cies guide and world checklist (Asher and Picker- conducted only for Peponapis sp., Apis mellifera, ing 2017). We collected two species of Peponapis, and Trigona fulviventris, because sample sizes were but due to the difficulty of identifying species in too low for the remaining species. In each plot, video recordings, we report visitation by bees in we examined all plants on the day of sampling the genus Peponapis, rather than by species. We and covered with a mesh bag five to ten large were able to separate Peponapis by sexual gender flower buds. The following day, upon opening, using the sexual characters antennae length flowers were exposed to natural floral visitation (longer in male bees) and presence of scopae in and assigned to one of the following six treat- female bees (Canto-Aguilar and Parra-Tabla 2000, ments according to the number of visits received Cane et al. 2011). by particular insect species: (1) one visit by female We calculated visitation rates (visits per flower Peponapis spp. (n = 16 plants), (2) one visit by per hour) for each pollinator species and obser- Trigona fulviventris (n = 13 plants), (3) one visit by vation period (i.e., for each flower filmed). We Apis mellifera (n = 28 plants), (4) three visits evaluated the foraging behavior of insect species by A. mellifera (n = 15 plants), (5) all visitors that contacted the reproductive organs of the excluded, a control for autonomous self-pollina- flower by assessing the duration in minutes of tion (n = 15 plants), (6) open pollination control each pollination event. in wet season (n = 28 plants), and (7) open polli- nation in dry season (n = 42 plants). We only con- Pollen loads on pollinators’ bodies ducted treatment number 5 (pollinator exclusion) To determine the capacity of different floral vis- during the wet season. We did not repeat this itors to carry pollen of C. moschata, we captured treatment in the following dry season because the visitors at staminate flowers (six species of flowers that received the exclusion treatment in
❖ www.esajournals.org 4 November 2018 ❖ Volume 9(11) ❖ Article e02506 DELGADO-CARRILLO ET AL. the wet season did not produce fruit. After floral was included as a random effect in the model. All visitation, flowers were labeled and re-bagged for bees contacted stigmas of pistillate flowers of the rest of the day, removing the bag the follow- C. moschata with the lower part of their body; thus, ing day upon flower senescence. In the case of for analyses, we used the sum of pollen loads from open-pollinated flowers, the bag was removed ventral abdomen and ventral torso. Because we before anthesis and the flower was marked. A only captured three species in both seasons (Apis week later, we counted the flowers that initiated mellifera, Agapostemon sp., Augochloropsis metallica), fruit development, and a month later, we col- we considered bees collected in the dry and wet lected mature fruits and counted all viable seeds seasons as separate entities in this statistical analy- in each fruit. Variation in sample sizes among sis; for example, we considered Apis mellifera in treatments was the result of different visitation wet season different from A. mellifera in dry sea- frequencies of the different bee species. son. To compare the relative contribution of the different pollinator species to fruit set and seed Statistical analyses set, we performed generalized linear models with To determine whether pollinator visitation GENMOD procedure in SAS version 9.4 (SAS rates and duration of pollinator visits differed 2014). The model used pollination treatment as the between pollinator species, seasons, and flower independent variable with the proportion of flow- gender, we used the GLIMMIX procedure in SAS ers that developed into fruit and number of seeds version 9.4 (SAS Institute Inc 2014). We consider produced per fruit as response variables. The anal- pollinator visitation rate as the number of visits ysis used a binomial distribution and a logit link by each pollinator to each flower per hour and function for fruit set and a normal distribution for the duration of pollinator visits as the time in seed set. We used the Tukey-adjusted P-values for minutes that each pollinator made to each flower. multiple comparisons. We conducted generalized linear mixed models to analyze: (1) the effect of season (dry or wet), RESULTS pollinator species and their interaction (fixed effects) on pollinator visitation rates, and dura- Pollinator community and foraging behavior tion of individual pollinator visits (response vari- The most frequent floral visitors in the wet ables); (2) the effect of flower gender, pollinator season were bees of the genus Peponapis, species, and their interaction on the same accounting for 92% and 95% of the total visits to response variables. In both analyses, field plot staminate and pistillate flowers, respectively. was included as a random effect in the model. Peak visitation occurred between 07:30 and We specified a Poisson distribution and a log link 08:30 hours, with female Peponapis leading the function for both response variables. We consid- visits to both staminate and pistillate flowers. In ered male and female Peponapis as separate contrast, in the dry season, the most frequent entities of the variable pollinator species to deter- visitor was Apis mellifera, accounting for 77% mine the contribution of each gender to pollina- and 70% of the total visits to staminate and tion. In all analyses, we specified the ILINK pistillate flowers, respectively; peak visitation option of the LS-MEANS statement to obtain in this season occurred between 09:00 and back-transformed least square means and a 10:00 hours (Fig. 1). Tukey adjustment for multiple comparisons. During the dry season, we observed 15 species To evaluate the capacity of different floral visi- of floral visitors; five of these were excluded from tors to carry pollen of C. moschata, we performed statistical analyses because they were all recorded a generalized linear mixed model with GLIM- a single time the same sampling day. In the wet MIX procedure in SAS version 9.4 (SAS Institute season, we recorded a subgroup of six pollinator 2014). The model included pollinator species as a species. We did not find significant differences in fixed effect and pollen count as response vari- pollinator visitation rates between seasons = = fi able. This analysis used a Poisson distribution (F(1,3) 2.33, P 0.2), but we found signi cant and a log link function, the ILINK option of the differences in pollinator visitation rates between = = LS-MEANS statement was used to obtain back- pollinator species (F(9,3) 13.08, P 0.02) and a transformed least square means, and field plot significant interaction between season and
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À À Fig. 1. Mean (ÆSE) number of pollinator visitsÁflower 1Áh 1 to female and male flowers of Cucurbita moschata throughout floral anthesis in (a) wet season and (b) dry season. Bee species not included in (a) (Apis mellifera, À À meliponini and halictid bees) and (b) (Peponapis and halictid bees) had less than one visitÁflower 1Áh 1. Melipo- nini bees include Scaptotrigona mexicana, Trigona fulviventris, and T. nigra.
= = = pollinator species (F(5,3) 13.32, P 0.02), with differences between pollinator species (F(9,3) Peponapis as the main floral visitor in the wet sea- 29.39, P = 0.009) and a significant interaction son, and Apis mellifera as the main visitor in the between flower gender and pollinator species = = dry season; pollinators from nine other species (F(9,3) 12.6, P 0.03),whereweobserveda were only present in the dry season (Fig. 2). strong preference for staminate flowers by Pepon- We did not find significant differences in apis and by pistillate flowers in Apis mellifera, Trig- pollinator visitation rates by flower gender ona fulviventris, and Scaptotrigona mexicana,andfor = = fi fl (F(1,3) 2.04, P 0.2), but we found signi cant staminate owers in Peponapis female bees (Fig. 3).
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À À Fig. 2. Mean (ÆSE) number of pollinator visitsÁflower 1Áh 1 by pollinator taxa in the wet season (white bars) and dry season (black bars). Different letters indicate significant differences between groups (P < 0.05) with Tukey’s ad hoc test.
We did not find significant differences in the flowering individuals of C. argyrosperma in the fl = fi duration of visits to owers by season (F(1,3) 1.57, wet season and it was dif cult to differentiate the P = 0.29), but we found significant differences pollen of each Cucurbita species, we report pollen = = fi between pollinator species (F(9,3) 42.8, P 0.005) counts for Cucurbita spp. We found signi cant dif- = and in the interaction between season and pollina- ferences among pollinator species (F(9,80) 674.56, = = < tor species (F(5,3) 10.45, P 0.04; Fig. 4). Both P 0.0001; Fig. 5). In the dry season, A. mellifera Apis mellifera and Peponapis made significantly carried pollen loads that were four times greater longer visits to flowersinthewetseasonthanin than the loads carried by this species in the wet the dry season (Fig. 4). We did not find significant season; other bees did not change their efficiency differences in the duration of flower visits by or were simply present in one season. The pollen fl = = ower gender (F(1,3) 6.42, P 0.08), nor in the load of Peponapis female bees was similar to the interaction between flower gender and pollinator pollen load of other pollinator species that carry = = species (F(8,3) 6.22, P 0.08), but we found sig- large amounts of pollen in their bodies. nificant differences in the duration of flower visits = = by pollinator species (F(9,3) 73.34, P 0.002). The Pollinator efficiency experiments duration of flower visits by A. mellifera was at least Due to the changes in pollinator assemblages three times higher than the duration of other polli- between seasons, we only performed efficiency nator species. experiments with Peponapis spp in the wet season and with Apis mellifera and Trigona fulviventris in Pollen load on pollinators’ body the dry season. We found significant differences We collected 93 individuals from six bee species. in fruit set between pollination treatments All the bees captured in staminate flowers had (v2 = 64.2, df = 6, P ≤ 0.0001). Flowers under pollen in some part of their body. Since we found complete pollinator exclusion and flowers
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À À Fig. 3. Mean (ÆSE) number of pollinator visitsÁflower 1Áh 1 by pollinator taxa in female (white bars) and male flowers (black bars). Different letters indicate significant differences between groups (P < 0.05) with Tukey’sad hoc test. exposed to a single visit of T. fulviventris did not three A. mellifera visits treatment was excluded produce any fruit. We did not find significant dif- from the statistical analysis due to the small sam- ferences in fruit set after one visit of Peponapis ple size (n = 2 fruits). female bees and open pollination, and these two treatments produced the highest fruit set. Fruit DISCUSSION set after one and three visits of A. mellifera was significantly lower than the fruit set of open-pol- Few studies have shown that species-rich linated flowers and the fruit set of one Peponapis insect communities enhance the pollination effi- visit treatment (Fig. 6). For seed production, we ciency of native plants and crops through com- collected a total of 56 fruits of C. moschata; on plementarity, where both the dominant and less average, fruits from open-pollinated flowers pro- abundant pollinator species contribute to reach- duced 538 Æ 32.4 seeds (n = 22) in the wet sea- ing a yield threshold (Hoehn et al. 2008, Winfree son and 510 Æ 29.8 seeds (n = 26) in the dry et al. 2018). Moreover, species turnover across season, fruits from the single female Peponapis landscapes can also be important to attain this visit produced 446 Æ 61.9 (n = 6) seeds, and threshold (Winfree et al. 2018). However, in fruits developed from flowers that received three some agricultural systems, fluctuations in the fre- A. mellifera visits produced 384 (Æ69.3, n = 2) quency of the most abundant pollinator species, seeds. There were no differences in seed number rather than changes in species richness, may per fruit between the single Peponapis visit treat- drive temporal variation in pollination services ment and the open pollination treatment in wet (Genung et al. 2017). This study showed that and dry seasons (v2 = 1.81, df = 2, P = 0.4). The temporal variation in the pollinator community
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À À Fig. 4. Mean (ÆSE) duration (min) of pollinator visitsÁflower 1Áh 1 by pollinator taxa in wet (white bars) and dry season (black bars). Different letters indicate significant differences between groups (P < 0.05) with Tukey’s ad hoc test. significantly affected the pollination efficiency of contributes to pollination services in other crops Cucurbita moschata crops between wet and dry (Greenleaf and Kremen 2006, Brittain et al. 2013). seasons in cultivated areas surrounded by tropi- Temporal variation in pollinator visitation and cal dry forest. In the wet season, native bees of efficiency determined the reproductive success of the genus Peponapis were the most frequent and C. moschata. In the wet season, Peponapis bees effective pollinators of C. moschata, with little visit C. moschata flowers early in the morning contribution from other bee species. In contrast, before other species arrive at flowers, removing in the dry season, Peponapis bees were scarce and and depositing more viable pollen than other Apis mellifera became the main floral visitor of pollinator species; furthermore, Peponapis bees C. moschata crops. The pollination efficiency had four times greater pollen loads and visitation results of our study indicate that three visits of rates to pistillate flowers than A. mellifera. These A. mellifera did not increase fruit set over one results suggest that when Peponapis bees are pre- visit of A. mellifera, but the fruit set of open polli- sent, they are the most effective pollinators of nation was similar in both seasons; therefore, in C. moschata. However, the importance of Pepon- the dry season, complementarity by other bee apis bees in the pollination of Cucurbita species is species contributes to fruit production in not consistent across the geographic distribution C. moschata crops. Similarly, complementarity by of these crops. In the Yucatan Peninsula in Mex- native bees in conjunction with A. mellifera ico and in western United States, the genus
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Fig. 5. Mean (ÆSE) number of Cucurbita pollen grains on the bodies of each pollinator taxon. White bars represent the pollinators in the wet season and black bars pollinators in the dry season. Different letters indicate significant differences between groups (P < 0.05) with Tukey ad hoc test.
Fig. 6. Mean fruit set (ÆSE) of pollinator efficiency treatments. Different letters indicate significant differences between treatments (P < 0.05) with Tukey ad hoc test. The treatments pollinator exclusion and one visit of Trigona fulviventris did not produce fruits.
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Peponapis is reported as one of the main pollina- shared evolutionary history between plants and tors of squash crops (Tepedino 1981, Canto-Agui- bees that has probably led to the observed syn- lar and Parra-Tabla 2000); however, at other sites chrony in their reproductive phenologies. in North America, Guatemala, and Brazil, this Bees of the genus Peponapis and squash crops group of bees is apparently poorly represented of the genus Cucurbita have their center of origin or not observed in squash crops (Serra and Cam- in Mexico and naturally occur throughout pos 2010, Petersen et al. 2013, Enr ıquez et al. Mesoamerica (Hurd et al. 1971, 1974, Lira-Saade 2015, Phillips and Gardiner 2015). One possible 1995, Ayala and Griswold 2012). Cultivated spe- explanation for the apparent incongruence in the cies of Cucurbita have been used by humans for importance of Peponapis bees for squash crops thousands of years, and the distributions of some from different geographic regions is that most Peponapis species have been associated with studies have not considered temporal variation human dispersal of squash crops (Nee 1990, Lira- in floral visitation to these crops. Saade 1995, Lopez-Uribe et al. 2016, Balvino- The phenology of Peponapis bees in seasonal Olvera et al. 2017). At present, these crops are environments is probably an important determi- dynamically cultivated in small orchards and nant of the temporal variation in pollinator fields, according to peasants’ necessities and assemblages documented in this study. As market prices in Mexico; thus, cultivated observed by Delgado-Carrillo et al. (2017), the squashes are not always available to Peponapis life cycle of Peponapis bees in the Central Pacific bees. Nevertheless, the strong interaction coast of Mexico is synchronized with the natural between Peponapis and Cucurbita species (both blooming period of squash crops in the wet sea- wild and cultivated) has resulted in high pollina- son. Species of Peponapis are reported as annuals; tion efficiency, as was demonstrated in this and for example, Peponapis pruinosa in North Eastern other studies between native bees and native United States overwinters as a prepupa in the crops (Tepedino 1981, Canto-Aguilar and Parra- soil, pupation begins in mid-June and adult Tabla 2000, Isaacs and Kirk 2010, Frier et al. activity ceases in early September (Mathewson 2016, Gibbs et al. 2016). Therefore, native species 1968, Julier and Roulston 2009). Active nests of are expected to be the most efficient pollinators Peponapis crassidentata and P. utahensis have been of native crops. described in the late wet season in Mexican dry As stated before, Cucurbita moschata crops are forests (Rozen and Ayala 1987, Delgado-Carrillo cultivated using artificial irrigation during the et al. 2017), and the few Peponapis individuals dry season, when annual species of Cucurbita observed during the dry season in this study and Peponapis bees do not naturally occur. The were probably the last adults of the previous absence of native effective pollinators would sug- year. Because both species of Peponapis at the gest a reduction in the fruit set of Cucurbita study site spend the majority of the dry season as moschata crops in the dry season. However, we a prepupa, they are not important pollinators of did not find significant differences in natural C. moschata crops during this season. Peponapis fruit set or seed production between the two sea- bees are fully dependent on the resources pro- sons. Our result suggests that introduced and vided by flowers of the genus Cucurbita for nutri- native bee species maintain pollination services tion of both larvae and adults (Hurd et al. 1971, for this crop during the dry season. Specifically, Delgado-Carrillo et al. 2017). Furthermore, the Apis mellifera is a less efficient pollinator than phenology of Peponapis is synchronized with the Peponapis at single flower visits, but low pollina- flowering phenology of the wild gourd C. argy- tion efficiency is compensated by its high visita- rosperma—a species that occurs along riverbanks tion rate and by the pollination effected by native and seasonal wetlands along the Pacific coast of halictid and stingless bees during the dry season. Mexico (Mariano and Dirzo 2002, Balvino-Olvera Africanized Apis mellifera colonized Mexico in et al. 2017). Similar synchronicity has been found 1986 and gradually expanded its prolific popula- for bat pollinators and the flowering phenology tions to most agroecosystems, natural areas, and of Bombacaceous trees in Neotropical dry forests even urban regions of Mexico (Lobo et al. 1989, (Lobo et al. 2003). Therefore, the association Lobo 1995, Quezada-Euan 2007). In our study between Peponapis and Cucurbita reflects a long region, we did not find managed hives near
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Cucurbita crops; therefore, honey bees pollinating Cucurbita produce unisexual staminate and pistil- Cucurbita flowers most likely come from feral late flowers, which are differentially visited by Africanized bee populations. A previous study Peponapis male and female bees; female bees vis- in the same region indicates that generalist polli- ited staminate flowers nearly twice as often as nators, such as Apis mellifera, are common in pistillate flowers, while male bees visited both areas under ecological succession and these flower genders at a low frequency. This result is abundant bees are also capable of providing pol- possibly explained by the high dependence of lination services to the plants in the surrounding female Peponapis bees to the pollen provided by tropical dry forest (Lopezaraiza-Mikel et al. staminate flowers, which they use to feed their 2013). This study shows that naturalized African- larvae (Hurd et al. 1971, Delgado-Carrillo et al. ized bees that inhabit natural forests in conjunc- 2017). There was also was a strong gender bias in tion with native bees allow offseason pollination Peponapis visitation rates to Cucurbita staminate of squash crops when Peponapis bees are absent flowers, where mean visitation rate by female or in low numbers. bees was 17 times higher than the visitation rate Another group of potential pollinators are the by male bees (Fig. 3). This result is in apparent native halictid bees, Ceratina bees, and stingless contradiction with a study that showed higher bees. Augochloropsis metallica and Agapostemon sp. visitation rates of P. pruinosa males than females visit squash flowers in both seasons, and they to flowers of C. pepo (Cane et al. 2011); however, carry large loads of Cucurbita pollen on their bod- the latter study did not differentiate visitation to ies. Although the pollination efficiency of these pistillate and staminate flowers and did not ana- bees was not measured in this study, halictid lyze the contribution of male and female bees to bees have been described in other studies as fre- the plant’s reproductive success. Female Pepon- quent visitors and efficient squash pollinators apis bees also visit pistillate Cucurbita flowers in (Ali et al. 2015). However, visitation rates of hal- search of high-energy sources, because pistillate ictid bees to Cucurbita moschata are low for both flowers of some Cucurbita species like C. pepo flower genders compared to Peponapis. Ceratina tend to produce higher quantities of nectar with bees carried pollen loads comparable to Pepon- greater sucrose concentration (Nepi et al. 2001). apis, but their visitation rates were low, only 10 Therefore, Peponapis female bees are the major individuals were captured in the wet season, and contributors to the pollination service and fruit no Ceratina bees were observed in video record- production of squash crops during the wet sea- ings. One species of stingless bee is apparently son. Differential use of floral resources by male an important pollinator of Cucurbita pepo in a and female pollinators of the same species has cloud forest in Guatemala, but the pollination been associated with differences in energetic efficiency of Peponapis was not measured at that requirements or feeding behaviors related to the site (Enr ıquez et al. 2015). In Chamela during the pollinator gender (e.g., Hymenoptera, Ne’eman dry season, we observed stingless bees taking et al. 2006, Lepidoptera, Alarcon et al. 2010, Dip- nectar from pistillate flowers and a few individu- tera, de Jager and Ellis 2012, hummingbirds, als visiting staminate flowers with low pollen Temeles et al. 2009). Likewise, in plant species loads on their bodies; however, the Trigona ful- with unisexual flowers, pollinators may prefer a viventris one-visit treatment did not produce any particular flower gender due to differential pro- fruits, suggesting that more than one visit is duction of floral rewards in pistillate and stami- required to develop a fruit, or that stingless bees nate flowers of the same plant species and this act as nectar and pollen robbers in squash flow- pollinator selectivity can influence the evolution ers. Halictid and Ceratina bees carry similar pol- of floral sexual dimorphism (e.g., Begonia, Le len loads as female Peponapis bees; however, they Corff et al. 1998, Ashman 2000). However, the have little impact on the pollination service pro- reciprocal impact that male and female pollina- vided to Cucurbita moschata due to their low tors of the same species have on male and female abundance. function of a particular plant species has been lit- Our study represents the first report of a vis-a- tle studied and deserves further attention. vis relationship of pollinator gender with respect Although fruit set and seed production are to plant gender. Monoecious plants of the genus similar in open pollination treatments in both
❖ www.esajournals.org 12 November 2018 ❖ Volume 9(11) ❖ Article e02506 DELGADO-CARRILLO ET AL. seasons, other studies have shown that pollen ACKNOWLEDGMENTS competition affects seed quality and progeny via- bility due to differences in the quality and quan- We thank two anonymous reviewers for providing tity of Cucurbita pollen (Quesada et al. 1991, feedback on the manuscript. We also thank P. Ramello, L. Alvarez, E. Paramo, E. P erez, G. Garc ıa, J. 1993, Winsor et al. 2000). Flowers of Cucurbita species are ephemeral, and their pollen loses via- Cristobal, S. Novais, A. De Novais, H. De Santiago, F. Parraguirre for laboratory and field assistance, Mar- bility within a few hours (Nepi and Pacini 1993, garito Alvarez-Jara for the elaboration of figure S1, Agbagwa et al. 2007, Franchi et al. 2014). Pepon- and Gumersindo Sanchez-Montoya, Ulises Olivares- fl apis bees, which arrive in great numbers at ow- Pinto, and Violeta Patino~ for technical assistance. We ers early in the morning when pollen is more thank the farmers of the region Costa Alegre who abundant and viable, might carry higher loads of supported this study. Oliverio Delgado-Carrillo is a viable pollen, which may in turn result in better PhD student from Programa de Doctorado en Cien- quality progeny. In contrast, Apis mellifera and cias Biom edicas, Universidad Nacional Autonoma de the other native bees in dry season arrive at flow- M exico (UNAM), fellowship 50222 from CONACyT. ers later in the day, a behavior that might be This work was supported by grants from DGAPA- associated with decreased progeny quality. This UNAM (PAPIIT # 212714 and IV200418 to MQ, hypothesis, which deserves experimental testing, IA207318 to SMR), CONACyT (CB-2009-131008, SAGARPA-CONACYT 291333 to MQ, CB-2014-01- predicts changes in the seed quality and progeny 241696 to MLM, Proyecto Laboratorio Nacional de viability of fruits produced at different time dur- Analisis y S ıntesis Ecologica 2015-250996, 2016- ing the day, and at different seasons by different 271449, 2017-280505, and 2018-293701 to MQ and types of pollinators. Furthermore, knowledge of SMR), and Programa Iberoamericana de Ciencia y pollen viability and seed quality in association Tecnolog ıa para el Desarrollo RED CYTED-SEPODI with progeny performance are key for the man- (417RT0527). ODC and MQ designed the study, ODC agement of native and introduced pollinators to collected the data and drafted the manuscript, ODC, obtain better seeds and fruits of economically MQ, and SMR performed analyses, and ODC, SMR, important crops. LA, RA, MLM, and MQ contributed with manuscript Finally, natural protected areas provide an writing. important pollination ecosystem service to crops because they provide nesting sites and floral LITERATURE CITED resources for squash pollinators. Riparian habi- tats and forest reserves can maintain native and Agbagwa, I. O., B. C. Ndukwu, and S. I. Mensah. 2007. feral pollinators of crops (Brito et al. 2017), and a Floral biology, breeding system, and pollination good example was shown for the provisioning of ecology of Cucurbita moschata (Duch. ex Lam) Duch. ex Poir. Varieties (Cucurbitaceae) from parts floral resources and nesting sites of Peponapis of the Niger Delta, Nigeria. Turkish Journal of Bot- crassidentata in the study area (Delgado-Carrillo any 31:451–458. et al. 2017). Currently, only 4% of this study area Alarcon, R., J. A. Riffell, G. Davidowitz, J. G. Hilde- is riparian habitat; thus it is crucial to protect this brand, and J. L. Bronstein. 2010. Sex-dependent environment for providing resources for bees variation in the floral preferences of the hawkmoth and other pollinator species (Sanchez-Azofeifa Manduca sexta. Animal Behaviour 80:289–296. et al. 2009). Ali, M., S. Saeed, A. Sajjad, and A. Akbar. 2015. Link- In Mexico, 85% of the crop species depend to ing pollination effectiveness and interspecific some degree on pollinators (Ashworth et al. displacement success in bees. Neotropical Ento- – 2009); therefore, it is necessary to study spatial mology 44:101 108. and temporal variation of pollinator communi- Armillas, P. 1949. Notas sobre sistemas de cultivo en Mesoam erica; cultivos de riego y humedad en la ties and the contribution of the different species cuenca del R ıo de las Balsas. Anales del Instituto of pollinators to the reproductive success of crop Nacional de Antropolog ıa e Historia 6:85–113. species. A better understanding of these ecologi- Artz, D. R., C. L. Hsu, and B. A. Nault. 2011. Influ- cal factors will allow improved management and ence of Honey Bee, Apis mellifera, hives and field conservation actions in agroecosystem land- size on foraging activity of native bee species in scapes that ensure the presence of insect pollina- pumpkin fields. Environmental Entomology 40: tors throughout the year. 1144–1158.
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Asher, J. S., and J. Pickering 2017. Discover life bee spe- Delgado-Carrillo, O., M. Lopezaraiza-Mikel, L. Ash- cies guide and world checklist (Hymenoptera: worth, R. Aguilar, J. A. Lobo, and M. Quesada. Apoidea: Anthophila). http://www.discoverlife.org/ 2017. A scientific note on the first record of nesting mp/20q?guide=Apoidea_species sites of Peponapis crassidentata (Hymenoptera: Api- Ashman, T.-L. 2000. Pollinator selectivity and its impli- dae). Apidologie 48:644–647. cations for the evolution of dioecy and sexual Dirzo, R., and C. Dom ınguez. 2002. Interacciones dimorphism. Ecology 81:2577–2591. planta-herb ıvoro en la selva baja caducifolia de Ashworth, L., M. Quesada, A. Casas, R. Aguilar, and Chamela. Pages 517–523 in F. A. Noguera, J. H. K. Oyama. 2009. Pollinator-dependent food pro- Vega-Rivera, A. N. Garc ıa-Aldrete, and M. Que- duction in Mexico. Biological Conservation 142: sada, editors. Historia natural de Chamela. Univer- 1050–1057. sidad Nacional Autonoma de M exico, Ciudad de Ayala, R. 2004. Fauna de abejas silvestres (Hymenop- M exico, M exico. tera: Apoidea) de Chamela. Pages 193–219 in A. N. Enr ıquez, E., R. Ayala, V. H. Gonzalez, and J. Nu nez-~ Garc ıa-Aldrete, editor. Artropodos de Chamela. Farfan. 2015. Alpha and beta diversity of bees and Instituto de Biolog ıa, Universidad Nacional their pollination role on Cucurbita pepo L. (Cucur- Autonoma de M exico, Cuidad de M exico, M exico. bitaceae) in the Guatemalan cloud forest. Pan-Paci- Ayala, R., and T. Griswold. 2012. Two new species of fic Entomologist 91:211–222. the bee genus Peponapis, with a key to the North Franchi, G. G., M. Nepi, and E. Pacini. 2014. Is flower/ and Central American species (Hymenoptera: Api- corolla closure linked to decrease in viability of dae: Eucerini). Revista Mexicana de Biodiversidad desiccation-sensitive pollen? Facts and hypotheses: 83:396–406. a review of current literature with the support of Balvino-Olvera, F. J., K. F. Sanchez-G omez, J. A. Lobo, some new experimental data. Plant Systematics G. Avila-Sakar, R. Cruz-Reyes, G. Sanchez-Mon- and Evolution 300:577–584. toya, Y. Herrer ıas-Diego, A. Gonzalez-Rodr ıguez, Free, J. B. 1993. Insect pollination of crops. Academic and M. Quesada. 2017. Latitudinal structured pop- Press, London, UK. ulations of the Mexican wild squash Cucurbita argy- Frier, S. D., C. M. Somers, and C. S. Sheffield. 2016. rosperma subsp. sororia revealed by microsatellite Comparing the performance of native and man- markers. Crop and Pasture Science 68:850–858. aged pollinators of Haskap (Lonicera caerulea: Brito, T. F., et al. 2017. Forest reserves and riparian cor- Caprifoliaceae), an emerging fruit crop. Agricul- ridors help maintain orchid bee (Hymenoptera: ture, Ecosystems & Environment 219:42–48. Euglossini) communities in oil palm plantations in Garibaldi, L. A., et al. 2013. Wild pollinators enhance Brazil. Apidologie 48:575–587. fruit set of crops regardless of honey bee abun- Brittain, C., N. Williams, C. Kremen, and A.-M. Klein. dance. Science 339:1608–1611. 2013. Synergistic effects of non-Apis bees and Genung, M. A., J. Fox, N. M. Williams, C. Kremen, J. honey bees for pollination services. Proceedings of Ascher, J. Gibbs, and R. Winfree. 2017. The relative the Royal Society of London B: Biological Sciences importance of pollinator abundance and species 280:20122767. richness for the temporal variance of pollination Bushmann, S. L., and F. A. Drummond. 2015. Abun- services. Ecology 98:1807–1816. dance and diversity of wild bees (Hymenoptera: Gibbs, J., E. Elle, K. Bobiwash, T. Haapalainen, Apoidea) found in lowbush blueberry growing and R. Isaacs. 2016. Contrasting pollinators and regions of Downeast Maine. Environmental Ento- pollination in native and non-native regions of mology 44:975–989. highbush Blueberry production. PLoS ONE 11: Cane, J. H., B. J. Sampson, and S. A. Miller. 2011. Polli- 1–24. nation value of male bees: the Specialist bee Pepon- Greenleaf, S. S., and C. Kremen. 2006. Wild bees apis pruinosa (Apidae) at summer squash (Cucurbita enhance honey bees’ pollination of hybrid sun- pepo). Environmental Entomology 40:614–620. flower. Proceedings of the National Academy of Canto-Aguilar, M. A., and V. Parra-Tabla. 2000. Impor- Sciences of USA 103:13890–13895. tance of conserving alternative pollinators: assess- Hoehn, P., T. Tscharntke, J. M. Tylianakis, and I. Stef- ing the pollination efficiency of the squash bee, fan-Dewenter. 2008. Functional group diversity of Peponapis limitaris in Cucurbita moschata (Cucur- bee pollinators increases crop yield. Proceedings of bitaceae). Journal of Insect Conservation 4:201–208. the Royal Society of London B: Biological Sciences Cuevas-Reyes, P., M. Quesada, and K. Oyama. 2006. 275:2283–2291. Abundance and leaf damage caused by Gall-indu- Hurd, P. D., E. G. Linsley, and A. E. Michelbacher. cing insects in a Mexican Tropical Dry Forest. 1974. Ecology of the squash and gourd bee, Pepon- Biotropica 38:107–115. apis pruinosa, on cultivated cucurbits in California
❖ www.esajournals.org 14 November 2018 ❖ Volume 9(11) ❖ Article e02506 DELGADO-CARRILLO ET AL.
(Hymenoptera: Apoidea). Smithsonian Institution Lobo, J. A., M. A. D. Lama, and M. A. Mestriner. 1989. Press, Washington, D.C., USA. Population Differentiation and Racial Admixture Hurd, P. D., E. G. Linsley, and T. W. Whitaker. 1971. in the Africanized Honeybee (Apis mellifera L.). Squash and Gourd Bees (Peponapis, Xenoglossa) and Evolution 43:794–802. the origin of the cultivated Cucurbita. Evolution Lobo, J. A., M. Quesada, K. E. Stoner, E. J. Fuchs, Y. 25:218–234. Herrer ıas-Diego, J. Rojas, and G. Sabor ıo. 2003. INEGI. 2009. Prontuario de informacion geogra fica Factors affecting phenological patterns of bomba- municipal de los Estados Unidos Mexicanos, La caceous trees in seasonal forests in Costa Rica Huerta, Jalisco. Clave geoestad ıstica 14043, M exico. and Mexico. American Journal of Botany 90: Isaacs, R., and A. K. Kirk. 2010. Pollination services 1054–1063. provided to small and large highbush blueberry Lopezaraiza-Mikel, M., et al. 2013. Phenological pat- fields by wild and managed bees. Journal of terns of tropical dry forests along latitudinal and Applied Ecology 47:841–849. successional gradients in the neotropics. Pages de Jager, M. L., and A. G. Ellis. 2012. Gender-specific 101–128 in A. Sanch ez-Azofeifa, J. S. Powers, G. W. pollinator preference for floral traits. Functional Fernandes, and M. Quesada, editors. Tropical dry Ecology 26:1197–1204. forests in the Americas: Ecology, conservation, and Julier, H. E., and T. H. Roulston. 2009. Wild bee abun- management. CRC Press, Boca Raton, Florida, dance and pollination service in cultivated pump- USA. kins: farm management, nesting behavior and Lopez-Uribe, M. M., J. H. Cane, R. L. Minckley, and B. landscape effects. Journal of Economic Entomology N. Danforth. 2016. Crop domestication facilitated 102:563–573. rapid geographical expansion of a specialist polli- Klein, A.-M., C. Muller,€ P. Hoehn, and C. Kremen. nator, the squash bee Peponapis pruinosa. Proceed- 2009. Understanding the role of species richness for ings of the Royal Society of London B: Biological crop pollination services. Pages 195–208 in S. Sciences 283:20160443. Naeem, D. E. Bunker, A. Hector, M. Loreau, and C. Mariano, N., and R. Dirzo. 2002. Cucurbita argyros- Perrings, editors. Biodiversity, ecosystem function perma ssp. sororia (L. H. Bailey) Merrick y Bates and human wellbeing: An ecological and economic (Cucurbitaceae). Aguichichi. Pages 167–170 in F. A. perspective. Oxford University Press, Oxford, UK. Noguera, J. H. Vega-Rivera, A. N. Garc ıa-Aldrete, Klein, A.-M., B. E. Vaissiere, J. H. Cane, I. Steffan- and M. Quesada, editors. Historia natural de Cha- Dewenter, S. A. Cunningham, C. Kremen, and T. mela. UNAM, Ciudad de Mexico, Mexico. Tscharntke. 2007. Importance of pollinators in Mathewson, J. A.. 1968. Nest construction and life his- changing landscapes for world crops. Proceedings tory of the eastern cucurbit bee, Peponapis pruinosa of the Royal Society B: Biological Sciences 274:303– (Hymenoptera: Apoidea). Journal of the Kansas 313. Entomological Society 41:255–261. Kremen, C., N. M. Williams, and R. W. Thorp. 2002. Millennium Ecosystem Assessment, editor. 2005. Crop pollination from native bees at risk from agri- Ecosystems and human well-being: synthesis. cultural intensification. Proceedings of the National Island Press, Washington, D.C., USA. Academy of Sciences of USA 99:16812–16816. Nee, M. 1990. The Domestication of Cucurbita (Cucur- Le Corff, J., J. Agren, and D. W. Schemske. 1998. Floral bitaceae). Economic Botany 44:56–68. display, pollinator discrimination, and female Ne’eman, G., O. Shavit, L. Shaltiel, and A. Shmida. reproductive success in two Monoecious Begonia 2006. Foraging by male and female solitary bees species. Ecology 79:1610–1619. with implications for pollination. Journal of Insect Lira-Saade, R. 1995. Estudios Taxonomicos y eco- Behavior 19:383–401. geogra ficos de las Cucurbitaceae latinoamericanas Nepi, M., M. Guarnieri, and E. Pacini. 2001. Nectar de importancia economica. Systematic and ecogeo- secretion, reabsorption, and sugar composition in graphic studies on crop gene pools 9. International male and female flowers of Cucurbita pepo. Interna- Plant Genetic Resources Institute, Rome, Italy. tional Journal of Plant Sciences 162:353–358. Lira-Saade, R., and S. Montes. 1992. Cucurbitas Nepi, M., and E. Pacini. 1993. Pollination, pollen viabil- (Cucurbita spp.). Pages 61–75 in E. Hernandez-Ber- ity and pistil receptivity in Cucurbita pepo. Annals mejo and J. Leon, editors. Cultivos marginados. of Botany 72:527–536. Otra Perspectiva de 1942. FAO/Jard ın Botanico, Petersen, J. D., S. Reiners, and B. A. Nault. 2013. Polli- Roma, Italia. nation services provided by bees in Pumpkin fields Lobo, J. A. 1995. Morphometric isozymic and mito- supplemented with either Apis mellifera or Bombus chondrial variability of Africanized honeybees in impatiens or not supplemented. PLoS ONE 8(7): Costa Rica. Heredity 75:133–141. e69819.
❖ www.esajournals.org 15 November 2018 ❖ Volume 9(11) ❖ Article e02506 DELGADO-CARRILLO ET AL.
Phillips, B. W., and M. M. Gardiner. 2015. Use of video SAS. 2014. The analysis for this paper was generated surveillance to measure the influences of habitat using SAS software, Version 9.4 of the SAS System management and landscape composition on polli- for WINDOWS. Copyright © 2014. SAS Institute nator visitation and pollen deposition in pumpkin Inc. SAS and all other SAS Institute Inc. product or (Cucurbita pepo) agroecosystems. PeerJ 3:e1342. service names are registered trademarks or trade- Potts, S. G., J. C. Biesmeijer, C. Kremen, P. Neumann, marks of SAS Institute Inc., Cary, North Carolina, O. Schweiger, and W. E. Kunin. 2010a. Global polli- USA. nator declines: trends, impacts and drivers. Trends Serra, B. D. V., and L. A. de O. Campos. 2010. Ento- in Ecology & Evolution 25:345–353. mophilic pollination of squash, Cucurbita moschata Potts, S. G., S. P. M. Roberts, R. Dean, G. Marris, M. A. (Cucurbitaceae). Neotropical Entomology 39:153– Brown, R. Jones, P. Neumann, and J. Settele. 2010b. 159. Declines of managed honey bees and beekeepers Temeles, E. J., C. R. Koulouris, S. E. Sander, and W. J. in Europe. Journal of Apicultural Research 49:15– Kress. 2009. Effect of flower shape and size on for- 22. aging performance and trade-offs in a tropical Quesada, M., C. D. Schlichting, J. A. Winsor, and A. G. hummingbird. Ecology 90:1147–1161. Stephenson. 1991. Effects of genotype on pollen Tepedino, V. J. 1981. The pollination efficiency of the performance in Cucurbita pepo. Sexual Plant Repro- squash bee (Peponapis pruinosa) and the honey bee duction 4:208–214. (Apis mellifera) on summer squash (Cucurbita pepo). Quesada, M., J. A. Winsor, and A. G. Stephenson. Journal of the Kansas Entomological Society 54 1993. Effects of pollen competition on progeny per- (2):359–377. formance in a heterozygous cucurbit. American Whitaker, T. W. 1974. Cucurbita. Pages 135–144 in R. C. Naturalist 142:694–706. King, editor. Handbook of genetics. Springer, New Quezada-Euan, J. J. G. 2007. A retrospective history of York, New York, USA. the expansion of Africanized honeybees in Mexico. Winfree, R., J. R. Reilly, I. Bartomeus, D. P. Cariveau, Journal of Apicultural Research 46:295–300. N. M. Williams, and J. Gibbs. 2018. Species turnover Rogers, S. R., D. R. Tarpy, and H. J. Burrack. 2014. Bee promotes the importance of bee diversity for crop species diversity enhances productivity and stabil- pollination at regional scales. Science 359:791–793. ity in a perennial crop. PLoS ONE 9:e97307. Winfree, R., N. M. Williams, J. Dushoff, and C. Kre- Rozen, J. G. Jr, and R. Ayala. 1987. Nesting biology of men. 2007. Native bees provide insurance against the squash bee Peponapis utahensis (Hymenoptera; ongoing honey bee losses. Ecology Letters 10:1105– Anthophoridae; Eucerini). Journal of the New York 1113. Entomological Society 95(1):28–33. Winsor, J. A., S. Peretz, and A. G. Stephenson. 2000. Sanchez-Azofeifa, G. A., M. Quesada, P. Cuevas-Reyes, Pollen competition in a natural population of A. Castillo, and G. Sanchez-Montoya. 2009. Land Cucurbita foetidissima (Cucurbitaceae). American cover and conservation in the area of influence of Journal of Botany 87:527–532. the Chamela-Cuixmala Biosphere Reserve, Mexico. ZEN. 2012. V. 1.1.2.0., 2011. Carl Zeiss Microscopy Forest Ecology and Management 258:907–912. GmbH, Jena, Germany.
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