Journal of Animal Behaviour and Biometeorology
https://www.jabbnet.com/article/doi/10.31893/jabb.23022
Journal of Animal Behaviour and Biometeorology
Research Article Open Access

Foraging patterns of bees in watermelon (Citrullus lanatus Thunb.) flowers in Panama

Juan Carlos Di Trani, Virginia Meléndez Ramírez, Anovel Barba, Yostin Añino

Downloads: 1
Views: 683

Abstract

The foraging patterns of bees in watermelon (Citrullus lanatus Thunb.) flowers were investigated in Los Santos, Panama, over a period of 84 observation days. The study aimed to identify the bee species visiting the flowers, their daily visitation rates, and the resources they foraged. The majority of visits were made by native bees, particularly stingless bees, suggesting their crucial role in pollinating watermelon crops in the area. The most frequently observed bee species visiting the flowers were N. perilampoides (58.7%), A. mellifera (23%), and P. peckolti (4%). Nectar was the primary resource foraged by most bees, with comparable visitation rates for both male (staminate) and female (pistillate) flowers. Honeybees allocated nearly half of their visits (47.7%) for pollen collection, and the majority of their daily visits occurred between 7:00 and 8:00 hours. In contrast, stingless bee visits peaked between 8:00 and 9:00 hours. Nectar visits were shorter in duration than pollen visits, with honeybees exhibiting the shortest durations when visiting watermelon flowers. Significant variations were observed in the daily foraging patterns among bee species during the 84-h observation period (Friedman P < 0.05). Additionally, bee characteristics such as size, color, and sociability, along with the time of day, significantly influenced flower visits for resources (GLMM P < 0.05). These findings contribute to the understanding of Central American bee species' behavior, aid in their conservation and management and have implications for enhancing fruit production in local watermelon crops.

Keywords

bee foraging, duration, nectar, pollen, visits, watermelon

References

Abou-Shaara HF, Owayss AA, Ibrahim YY, Basuny NK (2017) A review of impacts of temperature and relative humidity on various activities of honeybees. Insectes sociaux 64:455-463.

Abrol DP (2012) Pollination Biology. Springer, Dordrecht.

Adlerz WC (1966) Honeybee visit numbers and watermelon pollination. Journal of Economic Entomology 59:28-30.

ANAM. (2009) Atlas de las Tierras Secas y Degradadas de Panamá, Autoridad Nacional del Ambiente, República de Panamá.

Barba A, Espinosa J, Suris M (2015) Adopción de prácticas para el manejo agroecológico de plagas en la sandía (Citrullus lanatus Thunb.) en Azuero. Panamá. Revista de Protección Vegetal 30:104-114.

Bennett CF (1965) Beekeeping with stingless bees in western Panama. Bee World 46:23-24.

Bernauer OM, Tierney SM, Cook JM (2022) Efficiency and effectiveness of native bees and honeybees as pollinators of apples in New South Wales orchards. Agriculture, Ecosystems and Environment 337:108063.

Bishop JA, Armbruster WS (1999) Thermoregulatory abilities of Alaskan bees: effects of size, phylogeny, and ecology. Functional Ecology 13:711-724.

Bomfim IGA (2013) Uso de abelhas sem ferrão (Meliponinae: Apidae) em casa de vegetação para polinização e produção de frutos de minimelancia [Citrullus lanatus (Thunb.) Matsum. andNakai] com e sem semente. Dissertation, Universidad Federal do Ceará.

Bomfim IGA, Bezerra ADDM, Nunes AC, Freitas BM, Aragão FASD (2015) Pollination requirements of seeded and seedless mini watermelon varieties cultivated under protected environment. Pesquisa Agropecuária Brasileira 50:44-53.

Bonet FM, Vergara CH (2019) Abejas silvestres de un cafetal orgánico en Veracruz, México. Universidad de las Américas Puebla. Puebla, México.

Buchmann SL, Nabhan GP (2012) The forgotten pollinators. Island Press, Washington, DC.

Campbell JW, Daniels JC, Ellis JD (2018) Fruit set and single visit stigma pollen deposition by managed bumble bees and wild bees in Citrullus lanatus (Cucurbitales: Cucurbitaceae). Journal of Economic Entomology 111:989-992.

Campbell JW, Stanley-Stahr C, Bammer M, Daniels JC, Ellis JD (2019) Contribution of bees and other pollinators to watermelon (Citrullus lanatus Thunb.) pollination. Journal of Apicultural Research 58:597-603.

Cardoso MWR. (2017) Eficiência das abelhas sociais Melipona scutellaris na polinização de minimelancia em ambiente protegido. XIV Seminário Estudantil de pesquisa e Extensão – FAMAM.

Carr RV (1967) Factors affecting honeybee foraging behavior in watermelon, Citrullus lanatus (Thunb.) Mans. Dissertation, University of Arizona.

Chaves L (2013) Efeitos de abelhas na frutificação e qualidade de melancia (cv. Crimson Sweet) na região Central do estado do Piauí. Dissertation. Universidade Estadual Paulista.

Cook SM, Awmack CS, Murray DA, Williams IH (2003) Are honeybees’ foraging preferences affected by pollen amino acid composition? Ecological Entomology 28:622-627.

Cruz IAD (2020) Eficiência de ninhos-isca na atração e na obtenção de enxames, por nidificação espontânea, de abelhas sem ferrão amazônicas. Dissertation, Instituto Nacional de Pesquisas da Amazonia

Delaplane KS, Mayer DF (2000) Crop pollination by bees. CABI publishing, New York.

Di Trani JC, Ramírez VM, Añino Y, Barba A (2022) Environmental conditions and bee foraging in watermelon crops in Panama. Journal of Animal Behavior and Biometeorology 10:2234-2234.

Eckert CD, Winston ML, Ydenberg RC (1994) The relationship between population size, amount of brood, and individual foraging behavior in the honeybee, Apis mellifera L. Oecologia 97:248-255.

Engels W, Rosenkranz P, Engels E (1995) Thermoregulation in the nest of the Neotropical stingless bee Scaptotrigona postica and a hypothesis on the evolution of temperature homeostasis in highly eusocial bees. Studies on Neotropical fauna and Environment 30:193-205.

FAO (2020) Production Quantities of Watermelons by Country. Food and Agriculture Organization of the United Nations). FAOSTAT (Food and Agriculture Data. http://www.fao.org/faostat/en/#data/QC/visualize. Accessed in December 2020.

Fishbein M, Venable DL (1996) Diversity and temporal change in the effective pollinators of Asclepias tuberosa. Ecology 77:1061-1073.

Freitas L (2013) Concepts of pollinator performance: is a simple approach necessary to achieve standardized terminology? Brazilian Journal of Botany 36:3-8.

Galen C, Stanton ML (1989) Bumble bee pollination and floral morphology: factors influencing pollen dispersal in the alpine sky pilot, Polemonium viscosum (Polemoniaceae). American Journal of Botany 76:419-426.

Garantonakis N, Varikou K, Birouraki A, Edwards M, Kalliakaki V, Andrinopoulos F (2016) Comparing the pollination services of honeybees and wild bees in a watermelon field. Scientia Horticulturae 204:138-144.

Giannini TC, Cordeiro GD, Freitas BM, Saraiva AM, Imperatriz-Fonseca VL (2015) The dependence of crops for pollinators and the economic value of pollination in Brazil. Journal of Economic Entomology 108:849-857.

Gonzáles Betancourt VH, Gonzáles M, Cuellar Y (2009) Notas biológicas y taxonómicas sobre los abejorros del maracuyá del género Xylocopa (Hymenoptera: Apidae, Xylocopini) en colombia. Acta Biológica Colombiana 14:3-40.

Harder LD (1990) Behavioral responses by bumble bees to variation in pollen availability. Oecologia 85:41-47.

Heinrich B (1974) Thermoregulation in Endothermic Insects: Body temperature is closely attuned to activity and energy supplies. Science 185:747-756.

Heinrich B (1975) Energetics of pollination. Annual Review of Ecology and Systematics 6:139-170.

Heinrich B (1993) The hot-blooded insects: strategies and mechanisms of thermoregulation. Harvard University Press, Cambridge.

Henne CS, Rodriguez E, Adamczyk JJ (2012) A survey of bee species found pollinating watermelons in the lower Rio Grande valley of Texas. Psyche 2012:1-5.

Hrncir M, Maia-Silva C (2013) On the diversity of foraging-related traits in stingless bees. In: Vit P et al. (eds) Pot-Honey. Springer, New York, pp 201-215.

Hrncir M, Maia-Silva C (2013) The fast versus the furious—On competition, morphological foraging traits, and foraging strategies in stingless bees. In Vit P, Roubik DW (eds): Stingless bees process honey and pollen in cerumen pots. Facultad de Farmacia y Bioanálisis, Universidad de Los Andes, pp 1-13.

Ivey CT, Martinez P, Wyatt R. (2003) Variation in pollinator effectiveness in swamp milkweed, Asclepias incarnata (Apocynaceae). American Journal of Botany 90:214-225.

Jaffé R, Pope N, Carvalho AT, Maia UM, Blochtein B, de Carvalho CAL, Imperatriz-Fonseca VL (2015) Bees for development: Brazilian survey reveals how to optimize stingless beekeeping. PloS one 10: e0121157.

Kendall LK, Stavert JR, Gagic V, Hall M, Rader R (2022) Initial floral visitor identity and foraging time strongly influence blueberry reproductive success. Basic and Applied Ecology 60:114-122.

Lau JA, Galloway LF (2004) Effects of low-efficiency pollinators on plant fitness and floral trait evolution in Campanula americana (Campanulaceae). Oecologia 141:577-583.

Layek, U, Kundu A, Bisui S, Karmakar P (2021) Impact of managed stingless bee and western honeybee colonies on native pollinators and yield of watermelon: A comparative study. Annals of Agricultural Sciences 66:38-45.

MacInnis G, Forrest JR (2019) Pollination by wild bees yields larger strawberries than pollination by honeybees. Journal of Applied Ecology 56:824-832.

Malerbo-Souza DT, Tadeu AM, Bettini PC., de Toledo VDAA (1999) Importância dos insetos na produção de melancia (Citrullus lanatus Thunb.)-Cucurbitaceae. Acta Scientiarum. Agronomy 21:579-583.

Meléndez RV, Magaña RS, Parra TV, Ayala BR, Navarro GJ (2002) Diversity of native bee visitor of cucurbit crops (Cucurbitaceae) in Yucatán, México. Journal of Insect Conservation 6:135-147

Metzel R, Montagnini F (2014) From farm to forest: factors associated with protecting and planting trees in a Panamanian agricultural landscape. Bois and Forets Des Tropiques 322:3-15.

Michener CD, McGinley RJ, Danforth BN (1994) The Bee Genera of North and Central America (Hymenoptera: Apoidea). Smithsonian Institution Press, Washington, D.C.

Michener CD (1954) Bees of Panamá. Bulletin of the American Museum of Natural History 104:1-176.

Michener CD (2000) The bees of the world. JHU press, Baltimore.

Michener CD, Winston ML, Jander R (1978) Pollen manipulation and related activities and structures in bees of the family Apidae. The University of Kansas Science Bulletin 51:575.

Mosseler A, Major J, Ostaff D, Ascher J (2020) Bee foraging preferences on three willow (Salix) species: Effects of species, plant sex, sampling day and time of day. Annals of Applied Biology 177:333-345.

Nates-Parra G, Palacios E, Parra A (2008) Efecto del cambio del paisaje en la estructura de la comunidad de abejas sin aguijón (Hymenoptera: Apidae) en Meta, Colombia. Revista de Biología Tropical 56:1295-1308.

Nicholls E, Hempel de Ibarra N (2017) Assessment of pollen rewards by foraging bees. Functional Ecology 31:76-87.

Njoroge, GN, Gemmill B, Bussmann R, Newton LE, Ngumi VW (2004) Pollination ecology of Citrullus lanatus at Yatta, Kenya. International Journal of Tropical Insect Science 24:73-77.

Njoroge GN, Gemmill B, Bussmann R, Newton LE, Ngumi VM (2010) Diversity and efficiency of wild pollinators of watermelon (Citrullus lanatus (Thunb.) Mansf.) at Yatta (Kenya). Journal of Applied Horticulture 12:35-41.

Ostwald MM, Smith ML, Seeley TD (2016) The behavioral regulation of thirst, water collection and water storage in honeybee colonies. Journal of Experimental Biology 219:2156-2165.

Pereboom JJM, Biesmeijer JC (2003) Thermal constraints for stingless bee foragers: the importance of body size and coloration. Oecologia 137:42-50.

Pinkus-Rendon MA, Parra-Tabla V, Meléndez-Ramírez V (2005) Floral resource use and interactions between Apis mellifera and native bees in cucurbit crops in Yucatán, México. The Canadian Entomologist 137:441-449.

Pisanty G, Afik O, Wajnberg E, Mandelik Y (2016) Watermelon pollinators exhibit complementarity in both visitation rate and single‐visit pollination efficiency. Journal of Applied Ecology 53:360-370.

Rader R, Reilly J, Bartomeus I, Winfree R (2013) Native bees buffer the negative impact of climate warming on honeybee pollination of watermelon crops. Global change biology 19:3103-3110.

Rasheed S, Harder L (1997) Economic motivation for plant species preferences of pollen‐collecting bumble bees. Ecological Entomology 22:209-219.

Rodrigo Gomez S, Ornosa C, Garcia Gila J, Blasco-Aróstegui J, Selfa J, Guara M, Polidori C (2021) Bees and crops in Spain: an update for melon, watermelon and almond. Annales de la Société entomologique de France 57:12-28.

Roubik DW (1983) Nest and colony characteristics of stingless bees from Panama (Hymenoptera: Apidae). Journal of the Kansas Entomological Society 56:327-355.

Roubik DW (1992a) Stingless bees: a guide to Panamanian and Mesoamerican species and their nests (Hymenoptera: Apidae: Meliponinae). In: Quintero D, Aiello A (Eds), Insects of Panama and Mesoamerica, Oxford University Press, Oxford, pp 495-524.

Roubik DW (1992b) Ecology and natural history of tropical bees. Cambridge University Press, Cambridge.

Roubik DW (2006) Stingless bee nesting biology. Apidologie 37:124-143.

Roubik DW (2012) Ecology and Social Organization of Bees. John Wiley and Sons, Chichester.

Schmickl, T, Crailsheim K (2004) Inner nest homeostasis in a changing environment with special emphasis on honeybee brood nursing and pollen supply. Apidologie 35:249-263.

Schwarz HF (1934) The solitary bees of Barro Colorado Island, Canal Zone. American Museum Novitates 722:1-24.

Silva MD, Ramalho M, Monteiro D (2014) Communities of social bees (Apidae: Meliponini) in trap-nests: the spatial dynamics of reproduction in an area of Atlantic Forest. Neotropical Entomology 43:307-313.

Southwick EE, Heldmaier G (1987) Temperature control in honeybee colonies. Bioscience 37:395-399.

Souza FF, Malerbo-Souza DT (2005) Entomofauna visitante e produção de frutos em melancia (Citrullus lanatus Thunb.) –Cucurbitaceae. Acta Scientiarum. Agronomy 27:449-454.

Spicer EK (2007) Efficacy of honeybees and native bees as pollen vectors for watermelon (Citrullus lanatus) and some ecologic predictors of pollinator abundance. Dissertation, North Carolina State University.

Stanghellini MS, Ambrose JT, Schultheis JR (1998) Seed production in watermelon: a comparison between two commercially available pollinators. HortScience 33:28-30

Stanghellini MS, Schultheis JR, Ambrose JT (2002) Pollen mobilization in selected Cucurbitaceae and the putative effects of pollinator abundance on pollen depletion rates. Journal of the American Society for horticultural Science 127:729-736.

Taha EKA, Bayoumi YA (2009) The value of honeybees (Apis mellifera, L.) as pollinators of summer seed watermelon (Citrullus lanatus colothynthoides L.) in Egypt. Acta Biologica Szegediensis 53:33-37.

Tepedino VJ (1981) The pollination efficiency of the squash bee (Peponapis pruinosa) and the honeybee (Apis mellifera) on summer squash (Cucurbita pepo). Journal of the Kansas Entomological Society 54:359-377.

Tepedino V, Horn LA, Durham S (2016) Pollen removal and deposition by pollen-and nectar-collecting specialist and generalist bee visitors to Iliamna bakeri (Malvaceae). Journal of Pollination Ecology 19:50-56.

Thomson JD, Thomson BA (1992) Pollen presentation and viability schedules in animal-pollinated plants: consequences for reproductive success. In: Wyatt R (ed) Ecology and evolution of plant reproduction. Chapman and Hall, New York, pp 1-24.

Thomson JD (1986) Pollen transport and deposition by bumble bees in Erythronium: influences of floral nectar and bee grooming. The Journal of Ecology 74:329-341.

Thomson JD, Goodell K (2001) Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers. Journal of Applied Ecology 38:1032-1044.

Thomson JD, Plowright RC (1980) Pollen carryover, nectar rewards, and pollinator behavior with special reference to Diervilla lonicera. Oecologia 46:68-74.

Thorp RW (1979) Structural, behavioral, and physiological adaptations of bees for collecting pollen. Annals of the Missouri Botanical Garden 66:788–812

Thorp RW (2000) The collection of pollen by bees. Plant Systematics and Evolution 222:211-223.

Uruena A, Martínez-López V, de Jesús May-Itzá W, Quezada-Euán JJG, De la Rúa P (2022). Morphometric and genetic analyses show differentiation of the widely distributed stingless bee Nannotrigona perilampoides (Hymenoptera: Meliponini) across geographic regions in Mexico. Journal of Apicultural Research 61:609-618.

Vaudo AD, Patch HM, Mortensen DA, Tooker JF, Grozinger CM (2016) Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proceedings of the National Academy of Sciences 113: E4035-E4042.

Velthuis HH (1992) Pollen digestion and the evolution of sociality in bees. Bee world 73:77-89.

Vollet-Neto A, Menezes C, Imperatriz-Fonseca VL (2015) Behavioral and developmental responses of a stingless bee (Scaptotrigona depilis) to nest overheating. Apidologie 46:455-464.

Walters SA (2005) Honeybee pollination requirements for triploid watermelon. HortScience 40:1268-1270.

Westerkamp CH (1991) Honeybees are poor pollinators—why? Plant Systematics and Evolution 177:71-75.

Westerkamp CH (1996) Pollen in bee‐flower relations some considerations on melittophily. Botanica Acta 109:325-332.

Willmer PG (2011) Pollination and floral ecology. Princeton University Press, Princeton.

Willmer PG, Unwin DM (1981) Field analyses of insect heat budgets: reflectance, size, and heating rates. Oecologia 50:250-255.

Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72:1503-1507.

Young HJ, Dunning DW, von Hasseln KW (2007) Foraging behavior affects pollen removal and deposition in Impatiens capensis (Balsaminaceae). American Journal of Botany 94:1267-1271.

Zych M, Goldstein J, Roguz K, Stpiczyńska M (2013) The most effective pollinator revisited: pollen dynamics in a spring-flowering herb. Arthropod-Plant Interactions 7:315-322.


Submitted date:
05/06/2023

Accepted date:
06/29/2023

64ce8172a9539575503de442 jabbnet Articles
Links & Downloads

J. Anim. Behav. Biometeorol.

Share this page
Page Sections