Environmental conditions and bee foraging on watermelon crops in Panama
Juan Carlos Di Trani, Virginia Meléndez Ramírez, Yostin Añino, Anovel Barba
Abstract
Watermelon is a crop highly dependent on bees for pollination, and environmental conditions are some of the most important factors affecting bee foraging. In this study, we analyze the effect of environmental conditions on the behavior of the most common bees visiting flowers of watermelon crops in Panama. We recorded the number of visits, visit duration, and the corresponding environmental conditions during the visits. Environmental conditions affected the observed groups of bees differently: honey bee visit proportion was remarkably higher at low temperatures, solar radiation, wind speed, and high relative humidity, early in the morning when they made about 90% of their flower visits. The other observed bees showed a more homogenous behavior during the day, with peaks representing about 25-35% of the daily visits. Visit number showed a correlation with temperature for all the most common bees except Augochloropsis spp., with solar radiation for A. mellifera and Lasioglossum spp., with humidity for all except Lasioglossum spp., and with wind speed for all of the analyzed bees. Visit durations were remarkably longer in N. perilampoides early on the day. At the same time, the rest of the bees showed less pronounced duration peaks, reaching their maximum at intermediate values of environmental conditions. Visit duration on honeybees did not correlate with environmental factors, but it did for most other bees. Environmental conditions showed a strong effect on the bee foraging behavior, with each group of bees concentrating their activities in favorable conditions depending on their biology, establishing their daily foraging patterns.
Keywords
References
Abrol DP (1998) Foraging Ecology and Behaviour of the Alfalfa Pollinating Bee Species Megachile nana (Hymenoptera: Megachilidae). Entomologia generalis 233-237.
Abrol DP (2006) Diversity of pollinating insects visiting litchi flowers (Litchi chinensis Sonn.) and path analysis of environmental factors influencing foraging behaviour of four honeybee species. Journal of Apicultural Research 45:180-187.
Abrol DP (2010) Foraging behaviour of Apis florea F., an important pollinator of Allium cepa L. Journal of Apicultural Research 49:318-325.
Aleixo KP, Menezes C, Fonseca VLI, Da Silva CI (2017) Seasonal availability of floral resources and ambient temperature shape stingless bee foraging behavior (Scaptotrigona aff. depilis). Apidologie 48:117-127.
Alqarni AS (2015) Honeybee foraging, nectar secretion, and honey potential of wild jujube trees, Ziziphus nummularia. Neotropical entomology 44:232-241.
Alves LHS, Cassino PCR, Prezoto F (2015) Effects of abiotic factors on the foraging activity of Apis mellifera Linnaeus, 1758 in inflorescences of Vernonia polyanthes Less (Asteraceae). Acta Scientiarum Animal Sciences 37:405-409.
ANAM (2009) Atlas de las Tierras Secas y Degradadas de Panamá, Autoridad Nacional del Ambiente, República de Panamá.
Baird E (2020) Obstacle avoidance in bumblebees is robust to changes in light intensity. Animal cognition 23:1081-1086.
Baird E, Tichit P, Guiraud M (2020) The neuroecology of bee flight behaviours. Current Opinion in Insect Science 42:8-13.
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.
Barrows EM (1975) Mating behavior in halictine bees (Hymenoptera: Halictidae): III. Copulatory behavior and olfactory communication. Insectes Sociaux 22:307-331.
Barrows EM (1976) Mating Behavior in Halictine Bees (Hymenoptera: Halictidae) II. Microterritorial and Patrolling Behavior in♂♂ of Lasioglossum rohweri 1. Zeitschrift für Tierpsychologie 40:377-389.
Bennett CF (1965) Beekeeping with stingless bees in western Panama. Bee World 46:23-24.
Berry RP, Wcislo WT, Warrant EJ (2011) Ocellar adaptations for dim light vision in a nocturnal bee. Journal of Experimental Biology 214:1283-1293.
Bishop JA, Armbruster WS (1999) Thermoregulatory abilities of Alaskan bees: effects of size, phylogeny and ecology. Functional Ecology 13:711-724.
Blažytė-Čereškienė L, Vaitkevičienė G, Venskutonytė S, Būda V (2010) Honey bee foraging in spring oilseed rape crops under high ambient temperature conditions. Žemdirb 97:61-70.
Burdine JD, McCluney KE (2019) Differential sensitivity of bees to urbanization-driven changes in body temperature and water content. Sci Rep 9:1643.
Carr RV (1967) Factors affecting honey bee foraging behavior on watermelon, Citrullus lanatus (Thunb.) Mans. Dissertation, The University of Arizona.
Chang JJ, Crall JD, Combes SA (2016) Wind alters landing dynamics in bumblebees. Journal of Experimental Biology 219:2819-2822.
Clarke D, Robert D (2018) Predictive modelling of honey bee foraging activity using local weather conditions. Apidologie 49:386-396.
Combes SA, Dudley R (2009) Turbulence-driven instabilities limit insect flight performance. Proceedings of the National Academy of Sciences 106:9105-9108.
Contrera FAL, Imperatriz-Fonseca VL, Nieh JC (2004) Temporal and climatological influences on flight activity in the stingless bee Trigona hyalinata (Apidae, Meliponini). Revista Tecnologia e Ambiente 10:35-43.
Cooper PD, Schaffer WM, Buchmann SL (1985) Temperature regulation of honey bees (Apis mellifera) foraging in the Sonoran Desert. Journal of Experimental Biology 114:1-15.
Corbet SA (1990) Pollination and the weather. Israel Journal of Plant Sciences 39:13-30.
De Oliveira MAC (1973) Um método para a avaliação das atividade de vôo em Plebeia saiqui (Friese) (Hymenoptera, Meliponinae). Boletim de Zoologia e Biologia Marinha 30:625-631.
De Oliveira FL, Dias VHP, Da Costa EM, Filgueira MA, Sobrinho JE (2012) Influência das variações ambientales na atividade de vôo das abelhas jandairas Melipona subnitida Ducke (Meliponinae). Revista Ciência Agronômica 43:598-603.
Digby PS (1955) Factors affecting the temperature excess of insects in sunshine. Journal of Experimental Biology 32:279-298.
Dyer FC (1985) Nocturnal orientation by the Asian honey bee, Apis dorsata. Animal behaviour 33:769-774.
Erickson EH, Buchmann SL (1983) Electrostatics and pollination. Van Nostrand Reinhold Pub.
Fidalgo ADO, Kleinert ADMP (2007) Foraging behavior of Melipona rufiventris Lepeletier (Apinae; Meliponini) in Ubatuba, SP, Brazil. Brazilian Journal of Biology 67:133-140.
Gobatto AL, Knoll F (2013) Influence of seasonal changes in daily activity and annual life cycle of Geotrigona mombuca (Hymenoptera, Apidae) in a Cerrado habitat, São Paulo, Brazil. Iheringia. Série Zoologia 103:367-373.
Goodwin RM, Cox HM, Taylor MA, Evans LJ, McBrydie HM (2011) Number of honey bee visits required to fully pollinate white clover (Trifolium repens) seed crops in Canterbury, New Zealand. New Zealand Journal of Crop and Horticultural Science 39:7-19.
Gouw MS, Gimenes M (2013) Differences of the daily flight activity rhythm in two Neotropical stingless bees (Hymenoptera, Apidae). Sociobiology 60:183-189.
Greiner B, Cronin TW, Ribi WA, Wcislo WT, Warrant EJ (2007) Anatomical and physiological evidence for polarisation vision in the nocturnal bee Megalopta genalis. Journal of Comparative Physiology A 193:591-600.
Guibu LS, Imperatriz-Fonseca VL (1984) Atividade externa de Melipona quadrifasciata Lepeletier (Hymenoptera, Apidae, Meliponinae). Ciência e Cultura 36:623.
Hart GM, Eckhart VM (2010) Ecological separation in foraging schedule and food type between pollinators of the California wildflower, Clarkia xantiana ssp. xantiana. J Pollinat Ecol 2:13-20.
Heard TA, Hendrikz JK (1993) Factors influencing flight activity of colonies of the stingless bee Trigona carbonaria (Hymenoptera, Apidae). Australian Journal of Zoology 41:343-353.
Heinrich B (1993) The hot-blooded insects: strategies and mechanisms of thermoregulation. Springer Science & Business Media.
Herrera CM (1990) Daily patterns of pollinator activity, differential pollinating effectiveness, and floral resource availability, in a summer-flowering Mediterranean shrub. Oikos 277-288.
Hilário SD, Imperatriz-Fonseca VL, Kleinert A (2000) Flight activity and colony strength in the stingless bee Melipona bicolor bicolor (Apidae, Meliponinae). Revista brasileira de biologia 60:299-306.
Hilário SD, Imperatriz-Fonseca VL, Kleinert ADMP (2001) Responses to climatic factors by foragers of Plebeia pugnax Moure (in litt.) (Apidae, Meliponinae). Revista Brasileira de Biologia 61:191-196.
Hilário SD, de Fátima Ribeiro M, Imperatriz-Fonseca VL (2007) Efeito do vento sobre a atividade de vôo de Plebeia remota (Holmberg, 1903) (Apidae, Meliponini). Biota Neotropica 7:225-232.
Hrncir M, Maia-Silva C (2013) On the diversity of foraging-related traits in stingless bees. In Pot-Honey (pp. 201-215). Springer, New York, NY.
Iwama S (1977) A influência dos fatores climáticos na atividade externa de Tetragonisca angustula (Apidae, Meliponinae) Bol. Zool. Univ. S. Paulo 2:189-201.
Jander U, Jander R (2002) Allometry and resolution of bee eyes (Apoidea). Arthropod Structure & Development 30:179-193.
Kaluza BF (2017) Impacts of landscape resource diversity and availability on bee foraging and fitness. Dissertation, Universitätsbibliothek der Leuphana Universität Lüneburg.
Kapustjanskij A, Streinzer M, Paulus HF, Spaethe J (2007) Bigger is better: implications of body size for flight ability under different light conditions and the evolution of alloethism in bumblebees. Functional Ecology 21:1130-1136.
Kelber A, Warrant EJ, Pfaff M, Wallén R, Theobald JC, Wcislo WT, Raguso RA (2005) Light intensity limits foraging activity in nocturnal and crepuscular bees. Behavioral Ecology 17:63-72.
Kerfoot WB (1967) The lunar periodicity of Sphecodogastra texana, a nocturnal bee (Hymenoptera: Halictidae). Animal Behaviour 15:479-486.
Kleinert-Giovannini A (1982) Influence of climatic factors on flight activity of Plebeia emerina Friese (Hymenoptera, Apidae, Meliponinae) in winter. Revista Brasileira de Entomologia 26:13.
Linsley EG (1978) Temporal patterns of flower visitation by solitary bees, with particular reference to the southwestern United States. Journal of the Kansas Entomological Society 531-546.
Manetas Y, Petropoulou Y (2000) Nectar amount, pollinator visit duration and pollination success in the Mediterranean shrub Cistus creticus. Annals of Botany 86:815-820.
Meléndez RV (1997) Polinización & biodiversidad de abejas nativas asociadas a cultivos hortícolas en el estado de Yucatán, México. Dissertation, Universidad Autónoma de Yucatán, México.
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 & Forets des Tropiques 322:3-15.
Michener CD (1974) The social behavior of the bees: a comparative study (Vol. 73, No. 87379). Harvard University Press.
Michener CD (2000) The bees of the world (Vol. 1). JHU press.
MIDA (Ministerio de Desarrollo Agropecuario) 2017. https://www.mida.gob.pa/noticias_id_4799.html. Accessed Feb 2020.
Nikolova I, Georgieva N, Kirilov A, Miladenova R (2016) Dynamics of dominant bees-pollinators and influence of temperature, relative humidity and time of day on their abundance in forage crops in Pleven region, Bulgaria. Journal of Global Agriculture and Ecology 5:200-209.
Omoloye AA, Akinsola PA (2006) Foraging sources and effects of selected plant characters and weather variables on the visitation intensity of honeybee, Apis mellifera adansonii (Hymenoptera: Apidae) in the southwest Nigeria. J. Apic. Sci 50:39-48.
Pereboom JJM, Biesmeijer JC (2003) Thermal constraints for stingless bee foragers: the importance of body size and coloration. Oecologia 137:42-50.
Polatto LP, Chaud-Netto J, Alves-Junior VV (2014) Influence of abiotic factors and floral resource availability on daily foraging activity of bees. Journal of Insect Behavior 27:593-612.
Pick RA, Blochtein B (2002) Atividades de vôo de Plebeia saiqui (Holmberg) (Hymenoptera, Apidae, Meliponini) durante o período de postura da rainha e em diapausa. Revista Brasileira de Zoologia 19:827-839.
Raine NE, Chittka L (2007) Pollen foraging: learning a complex motor skill by bumblebees (Bombus terrestris). Naturwissenschaften 94:459-464.
Reddy PR, Rashmi T, Verghese A (2015) Foraging activity of Indian honey bee Apis cerana, in relation to ambient climate variables under tropical conditions. JEnvironBiol 36:577–81.
Richards MH (2004) Annual and social variation in foraging effort of the obligately eusocial sweat bee, Halictus ligatus (Hymenoptera: Halictidae). Journal of the Kansas Entomological Society 484-502.
Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press.
Roubik DW (1992) Stingless bees: a guide to Panamanian and Mesoamerican species and their nests (Hymenoptera: Apidae: Meliponinae). In: Quintero D and Aiello A (Eds). Insects of Panama and Mesoamerica, Oxford University Press, Oxford, UK, pp. 495-524.
Sadeh A, Shmida A, Keasar T (2007) The carpenter bee Xylocopa pubescens as an agricultural pollinator in greenhouses. Apidologie 38:508-517.
Sandoval-Molina MA, Flórez-Gómez NA, Pérez-Botello AM, Hinojosa-Díaz IA, Reyes-Tovar JM, Ayala R (2020) Effects of floral display and abiotic environment on the foraging activity of bees on Kallstroemia pubescens (Zygophyllaceae). Ethology Ecology & Evolution 32:551-571.
Sihag RC (1993) Behaviour and ecology of the subtropical carpenter bee, Xylocopa fenestrata F. 6. Foraging dynamics, crop hosts and pollination potential. Journal of Apicultural Research 32:94-101.
Smith AR, Kitchen SM, Toney RM, Ziegler C (2017) Is nocturnal foraging in a tropical bee an escape from interference competition? Journal of Insect Science 17:1-7
Soares KO, Lima MV, Evangelista-Rodrigues A, Silva AAF, Silva FJDA, Lima AIB, Da Costa CRG (2019) Factors influencing the foraging behavior of Trigona spinipes (Apidae, Meliponinae). Biological Rhythm Research 1-11.
Somanathan H, Borges RM, Warrant EJ, Kelber A (2008). Visual ecology of Indian carpenter bees I: light intensities and flight activity. Journal of Comparative Physiology A 194:97-107.
Somanathan H, Kelber A, Borges RM, Wallén R, Warrant EJ (2009) Visual ecology of Indian carpenter bees II: adaptations of eyes and ocelli to nocturnal and diurnal lifestyles. Journal of Comparative Physiology A 195:571-583.
Streinzer M, Huber W, Spaethe J (2016) Body size limits dim-light foraging activity in stingless bees (Apidae: Meliponini). Journal of Comparative Physiology A 202:643-655.
Sung I, Yamane S, Lu SS, Ho KK (2011) Climatological Influences on the Flight Activity of Stingless Bees (Lepidotrigona hoozana) and Honeybees (Apis cerana) in Taiwan (Hymenoptera, Apidae). Sociobiology 58:835-850.
Tarakini G, Chemura A, Tarakini T, Musundire R (2021) Drivers of diversity and community structure of bees in an agroecological region of Zimbabwe. Ecology and evolution 11:6415-6426.
Thakur SS (2007) Impact of ecological conditions on bee behaviour on different crops at Pantnagar, Uttrakhand. Journal of Entomological Research 31:247-250.
Thomson JD, Plowright RC (1980) Pollen carryover, nectar rewards, and pollinator behavior with special reference to Diervilla lonicera. Oecologia 46:68-74.
Veddeler D, Klein AM, Tscharntke T (2006) Contrasting responses of bee communities to coffee flowering at different spatial scales. Oikos 112:594-601.
Viana BF, Kleinert ADMP (2005) A community of flower-visiting bees (Hymenoptera: Apoidea) in the coastal sand dunes of northeastern Brazil. Biota neotropica 5:79-91.
Vicens N, Bosch J (2000) Weather-dependent pollinator activity in an apple orchard, with special reference to Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae and Apidae). Environmental Entomology 29:413-420.
Warrant EJ, Kelber A, Wallén R, Wcislo WT (2006) Ocellar optics in nocturnal and diurnal bees and wasps. Arthropod structure & development 35:293-305.
Warrant EJ (2008) Seeing in the dark: vision and visual behaviour in nocturnal bees and wasps. Journal of Experimental Biology 211:1737-1746.
Wcislo WT, Arneson L, Roesch K, Gonzalez V, Smith A, Fernández H (2004) The evolution of nocturnal behaviour in sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae:an escape from competitors and enemies? Biological Journal of the Linnean Society 83:377-387.
Willmer PG (1983) Thermal constraints on activity patterns in nectar‐feeding insects. Ecological Entomology 8:455-469.
Willmer PG, Unwin DM (1981) Field analyses of insect heat budgets: reflectance, size and heating rates. Oecologia 50:250-255.
Willmer PG, Stone GN (2004) Behavioral, ecological, and physiological determinants of the activity patterns of bees. Advances in the Study of Behavior 34:347-466.
Wratt E (1968) The pollinating activities of bumble bees and honeybees in relation to temperature, competing forage plants, and competition from other foragers. Journal of apicultural Research 7:61-66.
Yong X, Guo S (2016) The watermelon genome. In: Grumet R, Katzir N, Garcia-Mas J (Eds.) Genetics and Genomics of Cucurbitaceae. Springer, pp 199-210.
Submitted date:
08/04/2022
Reviewed date:
09/13/2022
Accepted date:
09/13/2022