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Male-fertile Potato Flowers are Selectively Buzz-Pollinated only by Bombus terricola Kirby in Upstate New York

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Abstract

Bombus terricola was the only pollinator of certified seed potatoes at four locations in the northern Adirondack Mountains, although seven other bumble bee species were present. Varieties yielding stainable, fertile pollen were preferred. Foragers sonicated 12-21 flowers per minute. Potatoes are also pollinated exclusively by bumble bees in central Europe, the Andes, the Himalayas, and the North American Great Lakes region. The conservation and management of selected bumble bee species are recommended, to ensure cross-pollination in potato fields.
252 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
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JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
66(2), 1993, pp. 252-254
Male-fertile Potato Flowers are Selectively Buzz-Pollinated
only by Bombus terricola Kirby in Upstate New York
Suzanne W. T. Batra
Bee Research Laboratory, Bldg. 476, Agricultural Research Service,
U.S. Department of Agriculture, Beltsville, Maryland 20705
abstract: Bombus terricola was the only pollinator of certified seed potatoes at four
locations in the northern Adirondack Mountains, although seven other bumble bee species
were present. Varieties yielding stainable, fertile pollen were preferred. Foragers sonicated
12-21 flowers per minute. Potatoes are also pollinated exclusively by bumble bees in central
Europe, the Andes, the Himalayas, and the North American Great Lakes region. The
conservation and management of selected bumble bee species are recommended, to ensure
cross-pollination in potato fields.
The potato is the only food crop among the eight major staples that is not a wind-pollinated grain;
annual worldwide production is over 279 M.t. (Simmonds, 1976). Cultivated potatoes originated in
the central Andes during 5000-2000 B.C. Because potato varieties evolved from complex hybridiza
tions among several diploid and polyploid species, floral sterility and variability are common (Sim
monds, 1976; Hawkes, 1979). Potatoes are usually propagated vegetatively; however, there is a need
to breed new varieties that will grow in warmer climates, produce more protein or other nutrients,
and have better disease resistance. For these reasons, and because potatoes grown from seed (true
potato seed) are less costly and less likely to transmit diseases than potatoes grown by vegetative
propagation (seed potatoes), research on the pollination of potato flowers has suddenly increased. As
in many other species of Solanum, potato flowers produce no nectar. The fragrant and showy, white,
lavender, yellow, blue, purple, or variegated flowers usually attract only insects that require pollen.
The large poricidal anthers form a conspicuous bright yellow cone that must be vibrated in order to
release their powdery pollen.
As early as 1881 (Free, 1970), Muller observed bumble bees collecting potato pollen in Europe, but
wind was long considered to be the most important pollinating agent. In 1947, Orsono-Mesa observed
two species of bumble bees pollinating potato flowers near Bogota, Colombia; he was the first to
describe the process of buzz-pollination or sonication, used by bees to vibrate anthers to release pollen;
he also noted that honey bees do not sonicate. Sanford and Hanneman (1981) found that honey bees
and Bombus fervidus (F.) were not attracted to potato flowers during cage trials, but that B. impatiens
Cr. effectively pollinated potatoes in Wisconsin fields, where they avoided cultivars that yielded sterile
pollen. In Peru, bumble bees pollinated 6-7 potato flowers per minute (White, 1983), and Bombus
Accepted for publication 20 December 1992.
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VOLUME 66, NUMBER 2 253
sp. buzz-pollinated potatoes in the Indian Himalayas (Birhman, 1988). Thus the potato everywhere
is clearly a specialized bumble bee flower. Arndt et al. (1990) confirmed that unspecified bumble bees
prefer clones that yield fertile pollen; they tend to work a series of flowers within such a clone before
moving to another clone. Bumble bees can assess the pollen yields of other species of Solanum
(Buchmann and Cane, 1989), as well as other plants (Harder, 1990), and they quickly alter their
behavior to maximize foraging efficiency. Arndt et al. (1990) showed that bumble bees could pref
erentially select fertile (stainable) pollen, which is presumably more nutritious for bees than sterile
(nonstaining) pollen.
In 1990 and 1991,1 studied pollination in fields of certified seed potatoes. These are propagated as
disease-free stock in isolated areas of the northern Adirondack Mountains, surrounded by boreal
forest, with a 100-day growing season (Thompson, 1966). Eight varieties and numerous pollinators
were surveyed near Gabriels, Rainbow Lake, Lake Placid, and Vermontville, N.Y. At all locations,
B. terricola was the only potato pollinator, although seven other bumble bee species live in the area:
B. vagans Sm., B. perplexus Cr. (both abundant), B. borealis Kby., B. bimaculatus Cr., B. affinis Cr.,
B. fervidus, and B. ternarius Say. These other species visited forbs and crops growing next to the potato
fields, but none was attracted to potato flowers, which even attracted a few pollen-scavenging or stigma
licking syrphids, wasps, and Dialictus and Andrena bees.
The B. terricola foragers were highly selective. They preferentially visited these cultivars: 'NY79',
with very fragrant, sparse, small cream-colored flowers (at a rate of 12-21 flowers visited per minute);
'Superior', with numerous large, violet flowers (12-19/min); 'Steuben (NY81)\ with white flowers
(12/min); and 'Allegheny', with violet flowers (16/min). Even when grown next to preferred varieties
and well within the bees' flight patterns, the cultivars 'Green Mountain' with white flowers, 'Russet'
with pale violet flowers and 'Atlantic' with pale lavender flowers were never visited. Several hundred
pollen grains per cultivar were stained with lactophenol-cotton blue. Varieties that were visited by
the bumble bees yielded 50-90% normal pollen grains that were plump and stained; the bees avoided
varieties that yielded 5-20% normal pollen grains and 80-95% shriveled, non-staining grains. This
confirms the findings of Arndt et al. (1990). Since they did not alight on the flowers, it is unknown
how the bees could determine the quality of the pollen grains from a distance.
Individual foragers varied considerably in speed of flight, directionality, and erratic movements
even when working a single preferred variety. Bees ranged from being flighty, not permitting close
observation, to being more placid. Foragers closely inspected (hovered), but did not alight on, 10
50% of open flowers, although adjacent similar flowers on the same plants were visited. Some indi
viduals tended to work down rows, but others readily crossed rows, often skipping several. Apparently
suitable plants in their flight paths seemed to be haphazardly omitted. For example, one bee pollinated
39 flowers in six rows occupying 3 m2 during 2.5 min. Bees worked up-, down- and crosswind. In
order to release the pollen, foragers grasped anther cones and emitted 1-4 sharp buzzes of about one
second each, audible as far as 3 m away; many bees rotated clockwise or counterclockwise while
buzzing, but some did not rotate.
Bumble bees carrying potato pollen visited various forbs for nectar. Late in the season, when
buckwheat, goldenrod, hardhack, and sunflowers began to bloom, B. terricola abandoned the potato
flowers in favor of these newly abundant, competing pollen sources.
Worthwhile future research would include the management of bumble bees for potato pollination;
pollinators for cultivars grown where bumble bees do not live; why only some species of bumble bees
pollinate potatoes; and how bumble bees can determine the condition of pollen from a distance.
acknowledgments: I thank B. Melching of the Uihlein Farm of Cornell University, Lake Placid,
N.Y.; D. Tucker, Tucker Farms, Gabriels, N.Y.; and S. Slack, Cornell University, for information
and assistance. Comments and suggestions by E. Barrows, of Georgetown University and M. Stoetzel
of USDA improved this manuscript.
Arndt, G. C, J. L. Rueda, H. M. Kidane-Mariam, and S. J. Peloquin. 1990. Pollen fertility in relation
to open pollinated true seed production in potatoes. American Potato Journal 67:499-505.
Birhman, R. K. 1988. Pollination mechanisms in Solanum chacoense Bitt. Acta Bot. Indica 16:
89-91.
Buchmann, S. L., and J. H. Cane. 1989. Bees assess pollen returns while sonicating Solanum flowers.
Oecologia 81:289-294.
Free, J. B. 1970. Insect Pollination of Crops. Academic Press, New York. 544 pp.
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254 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
Harder, L. D. 1990. Behavioral responses by bumble bees to variation in pollen availability. Oecologia
85:41-47.
Hawkes, J. G. 1979. Evolution and polyploidy in potato species. In J. G. Hawkes, R. N. Lester, and
A. D. Skelding (eds.), The Biology and Taxonomy of the Solanaceae, pp. 637-647. Academic
Press, London.
Osorno-Mesa, H. 1947. Observaciones antecologicas sobre recoleccion de polen por vibracion.
Caldasia 4:465-467.
Sanford, J. C. and R. E. Hanneman. 1981. The use of bees for the purpose of intermating in potato.
American Potato Journal 58:481-485.
Simmonds, N. W. 1976. Potatoes. In N. W. Simmonds (ed.), Evolution of Crop Plants, pp. 279
283. Longman, London.
Thompson, J. H. 1966. Geography of New York State. Syracuse University Press, Syracuse. 543 pp.
White, J. W. 1983. Pollination of potatoes under natural conditions. CIP Circular 11(2): 1-2. Inter
national Potato Center, Lima, Peru.
JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
66(2), 1993, pp. 254-256
Colonization of Grass Germplasm Nurseries by Diuraphis noxia
(Mordvilko) (Homoptera: Aphididae)
Stephen L. Clement, Donald G. Lester, and David M. Stout
Agricultural Research Service, U.S. Department of Agriculture, and
Regional Plant Introduction Station, Washington State University,
Pullman, Washington 99164
abstract: Russian wheat aphid (RWA), Diuraphis noxia (Mordvilko), colonized grass
germplasm nurseries maintained by the Western Regional Plant Introduction Station
(WRPIS) in southeastern Washington. Although most accessions exhibited little or no
RWA-induced damage, 22 accessions in the genera Agropyron, Elytrigia, Leymus, Ros
traria, Stipa, and Heteranthelium required an application of a foliar insecticide (dimethoate)
to suppress damaging RWA populations. This study demonstrated that seed-regeneration
protocol at WRPIS should include routine surveys of grass nurseries to detect germplasm
at risk to colonization and damage by RWA.
The Western Regional Plant Introduction Station (WRPIS) at Pullman, Washington, is responsible
for maintaining major germplasm collections of cool-season perennial grasses. Every year, WRPIS
personnel establish grass nurseries in southeastern Washington to regenerate seed of accessions low
in viability and supply. It is imperative that these nurseries at Pullman and the WRPIS research
station at Central Ferry, Washington, be protected from insect pests and diseases that might adversely
affect plant health.
The Russian wheat aphid (RWA), Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), was first
detected in grass plots at Central Ferry in 1988 (Clement et al., 1990), one year after it was discovered
attacking small grains in southeastern Washington (Pike and Suomi, 1988). In 1989, damaging pop
ulations of RWA in a Central Ferry nursery had to be suppressed with an insecticide (Clement, unpubl.
data). This event, together with the knowledge that more than 140 graminoid species were recorded
as RWA host plants (Pike et al., 1991), including many cool-season perennial grasses (Webster et al.,
1987; Kindler and Springer, 1989; Clement et al., 1990), suggested that the RWA had the potential
to adversely affect WRPIS seed-increase activities at Central Ferry. Noting this potential problem, we
set out to record the incidence of RWA on diverse grass taxa in nurseries at Central Ferry in 1990
and 1991.
In this communication, the colonization of WRPIS grass nurseries by RWA and insecticidal control
of damaging populations is documented. The implications of our findings to grass seed regeneration
activities at Central Ferry are also briefly discussed.
Accepted for publication 16 October 1992.
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... This specific plant-bee mechanism is called "buzz pollination" (Buchmann and Hurley, 1978;Buchmann, 1983), meaning bees use their thoracic muscles to produce very high frequency vibrations that expels pollen from the anthers. Moreover, bumblebees preferentially visit the flowers of potato cultivars that produce viable pollen grains instead of cultivars that produce primarily unviable, shrunken pollen grains (Batra, 1993). Since potato flowers do not produce nectar, honeybees (Apis mellifera L.) and Bombus fervidus Fabricius are not pollinators of potato (Sanford and Hanneman, 1981). ...
... It was observed that bumblebees are more likely to visit plants at the edges of plots as opposed to their centres, allowing them to stay closer to their nests (Batra, 1993;Free and Butler, 1959;McPartlan and Dale, 1994). Highest levels of berry formation were also recorded at the edges of plots, compared with the centre, suggesting that bumblebee activity was a contributing factor to pollination. ...
... Highest levels of berry formation were also recorded at the edges of plots, compared with the centre, suggesting that bumblebee activity was a contributing factor to pollination. Bumblebees will selectively visit different potato cultivars, preferring those with fertile pollen (Arndt et al., 1990;Batra, 1993;Sanford and Hanneman, 1981). ...
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The present technical report analysed the possible sources for potential cross-pollination with GM potato and adventitious admixture of GM potato material such as seeds and pollen and presents consensually agreed by TWG for Potato best practices for coexistence. The terms of reference for this review are presented in Section 1. The scope of the Best Practice Document is coexistence in potato production in the EU. It includes the coexistence between GM potato cultivation and honey production.
... This specific plant-bee mechanism is called "buzz pollination" (Buchmann and Hurley, 1978;Buchmann, 1983), meaning bees use their thoracic muscles to produce very high frequency vibrations that expels pollen from the anthers. Moreover, bumblebees preferentially visit the flowers of potato cultivars that produce viable pollen grains instead of cultivars that produce primarily unviable, shrunken pollen grains (Batra, 1993). Since potato flowers do not produce nectar, honeybees (Apis mellifera L.) and Bombus fervidus Fabricius are not pollinators of potato (Sanford and Hanneman, 1981). ...
... It was observed that bumblebees are more likely to visit plants at the edges of plots as opposed to their centres, allowing them to stay closer to their nests (Batra, 1993;Free and Butler, 1959;McPartlan and Dale, 1994). Highest levels of berry formation were also recorded at the edges of plots, compared with the centre, suggesting that bumblebee activity was a contributing factor to pollination. ...
... Highest levels of berry formation were also recorded at the edges of plots, compared with the centre, suggesting that bumblebee activity was a contributing factor to pollination. Bumblebees will selectively visit different potato cultivars, preferring those with fertile pollen (Arndt et al., 1990;Batra, 1993;Sanford and Hanneman, 1981). ...
... Presence of insects is imperative in facilitating cross-breeding and selfing in potato. Bumblebee species like Bombus terricola and B. impatiens are particularly good pollinators for potatoes [68,69]. European honey bee (Apis mellifera) and B. fervidus do not contribute to the pollination of potato, as the flowers are devoid of nectar [70]. ...
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... Visits to less productive flowers are briefer and do not involve collection of pollen to the pollen baskets." Bumblebees are remarkably selective, preferentially visiting plants with abundant, healthy pollen and avoiding those that produce little or shriveled pollen (Sanford and Hanneman 1981;Batra 1993). The means that bees use to determine the quality of pollen grains from a distance is unknown. ...
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... Batra 1993;Skogsmyr 1994;Chumbiauca et al. 2004;De Azeredo et al. 2006;Scurrah et al. 2008De igual manera, es poco lo que se conoce sobre el efecto de la intervención antrópica en estos agroecosistemas, en especial sobre las poblaciones de insectos benéficos (como los polinizadores), a pesar de que en teoría toda alteración en los ecosistemas agrícolas puede ocasionar cambios en la composición y estructura de las comunidades de insectos asociados a estos (Odum y Barrett 2005) y pese a que el conocimiento sobre la conformación de las redes abeja-planta es importante para el desarrollo de programas de conservación y manejo de dichos polinizadores y de la biodiversidad de una zona de cultivo en general (Ramalho et al. 1990;Carreck y Williams 1998;Nates-Parra y González 2000;Aizen et al. 2002;Albuquerque et al. 2006).En este trabajo se realizó un inventario de abejas asociadas a cultivos de papa en el departamento de Antioquia acompañado de un análisis de la estructura de sus poblaciones, con el ánimo de avanzar en el conocimiento de la melitofauna asociada a cultivos de papa en los diferentes tipos de uso del suelo encontrados en el país y además, de analizar el comportamiento de los ensamblajes de abejas en estos escenarios. ...
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Pollen-collecting bumble bees (Bombus spp.) detect differences between individual flowers in pollen availability and alter their behavior to capitalize on rewarding flowers. Specific responses by bees to increased pollen availability included: longer visits to flowers; visits to more flowers within an inflorescence, including an increased frequency of revisits; an increased likelihood of grooming while the bee flow between flowers within the inflorescence; and more protracted inter-flower flights, probably because of longer grooming bouts. The particular suite of responses that a bee adopted depended on the pollen-dispensing mechanism of the plant species involved. Bees buzzed previously-unvisited Dode-catheon flowers longer than empty flowers. In contrast, pollen availability did not significantly affect the duration of visits to Lupinus flowers, which control the amount of pollen that can be removed during a single visit. Simulation results indicate that the observed movement patterns of bumble bees on Lupinus inflorescences would return the most pollen per unit of expended energy. The increased foraging efficiency resulting from facultative responses by bees to variation in pollen availability, especially changes in the frequency and intensity of grooming, could correspondingly decrease pollen dispersal between plants.
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The pollination behavior of bumblebees and honey bees was studied on potato flowers in screened enclosures and in the field. In enclosures, the domestic honey bee (Apis mellifera L.) and the bumblebee species, Bombus fervidus Fabricius, seemed to lack any "cue" to initiate visitation of the flowers. When honey was placed on a few flowers, visitation was stimulated. The honey bee tore and chewed at the anther cone to collect pollen, while B. fervidus probed for nectar which was not present. Shortly afterward, both species ceased visitation and could not be induced to visit further, regardless of the honey stimulus. Neither species was effective as a pollinator. It is concluded that neither species will be useful for large-scale crossing of potato populations. However, another bumblebee species, Bombus impatiens Cresson, is very effective in pollinating potatoes in the field. Manipulating the behavior of such indigenous populations of bumblebees is likely to be the most effective method of exploiting insect pollination in the potato.
Evolution and polyploidy in potato species
  • J G Hawkes
Hawkes, J. G. 1979. Evolution and polyploidy in potato species. In J. G. Hawkes, R. N. Lester, and A. D. Skelding (eds.), The Biology and Taxonomy of the Solanaceae, pp. 637-647. Academic Press, London.
Observaciones antecologicas sobre recoleccion de polen por vibracion
  • H Osorno-Mesa
Osorno-Mesa, H. 1947. Observaciones antecologicas sobre recoleccion de polen por vibracion. Caldasia 4:465-467.
Department of Agriculture, and Regional Plant Introduction Station
  • L Stephen
  • Donald G Clement
  • David M Lester
Stephen L. Clement, Donald G. Lester, and David M. Stout Agricultural Research Service, U.S. Department of Agriculture, and Regional Plant Introduction Station, Washington State University,