Thrips and pollination
Dawn Frame, CNRS, UMR-AMAP, France
Kirk (1997) distinguished “thripophily”, a suite of characters defining an angiosperm pollination syndrome, and the following revised version includes: flowers small- to medium-sized, white to yellow or greenish often tipped with pink, pleasantly scented, sometimes borne in compact blossoms or if singly, opening successively, sometimes in the form of sheltering globose or urceolate flowers, blossoms providing minute quantities of nectar and small- to medium-sized pollen grains. However, there are numerous exceptions. Some of these characters overlap with those found in other pollination syndromes, particularly beetle or “cantharophily”, and small to medium-sized beetles are sometimes co-pollinators along with thrips.
Thrips can detect color and scent in flight, and actively fly short distances in response to these and possibly other cues such as form. Location of hosts over long distances is achieved by using a combination of active and passive dispersal on wind currents. So-called “rewards” associated with thrips pollination include: pollen, nectar, and possibly other epidermal cell contents, brood sites, heat, protection and mating opportunities. Thrips can manipulate pollen of many sizes, sculptures and textures for feeding, and female thrips will produce more eggs after a pollen meal. The pollen grains that thrips inadvertently carry are relatively small, either dry or somewhat sticky. Some grooming of grains occurs before thrips fly and other grains are also probably lost in flight.
Pollination of dioecious, putatively andro-dioecious and monoecious plants by thrips involves an intimate relationship between the pollinator’s life-cycle and the plant’s reproductive stage (see General Diagram above). Female and male thrips visit male blossoms at anthesis cued by scent, color and possibly form. They feed on pollen and mate. Gravid females primarily oviposit here or on other male anthesis blossoms but can also move to preanthesis male blossoms for ovipositing. Rapid build up of thrips populations can occur on male blossoms alone or on sterile (but usually nutritive) preanthesis male blossom appendages, prior to female blossom anthesis. Female and male thrips visit female blossoms attracted by scents and colors similar to male blossoms, and here they encounter minor rewards such as minute amounts of nectar. In this “deceitful” system, adult thrips of both sexes do not remain long on female blossoms, but their passage allows pollen transfer. Larvae develop in male preanthesis and anthesis blossoms, 2nd instar and propupae drop to the ground either directly or when senescent male blossoms abscise. Flowering or “coning” and the life-cycle of thrips are synchronized. For dioecious plants, cross-pollination (xenogamy) may be achieved and for monoecious plants, this can lead to either geitonogamy or xenogamy. These relationships have been studied for Cycadothrips albrechtii on Macrozamia macdonnellii, an Australian cycad (Mound & Terry 2001), also Thrips antiaropsidis on Antiaropsis decipiens, a New Guinea forest tree that is related to Fig trees (Zerega et al. 2004).
Common variations on this scheme include the following. Gravid females of a species of Dolichothrips oviposit in both male and female blossoms on Macaranga hullettii (Moog et al. 2002), and in related Macaranga species pupation can occur within blossoms (Fiala et al. 2011). Aggregating males of Brooksithrips chamaedoreae attract females to female blossoms on several Chamaedorea palm species, presumably by producing an aggregation pheromone (Morgan 2007). Temperature is a modulator of behavior and stimulator of development in Cycadothrips species on thermogenic cones of Macrozamia lucida and M. macleayi (Terry et al. 2004).
Thrips-pollination of cosexual hermaphroditic plants is less studied. The pollination system of Erica tetralix and Calluna is similar to the one outlined above (Hagerup & Hagerup 1953). However, the flowers mature sequentially on shoots, and adult thrips of both sexes as well as larvae move from flower to flower. Some fall with senescent flowers and pupate beneath the plants. Only females are winged in this thrips, Ceratothrips ericae, and these fly to flowers of neighboring conspecific plants. Similar sequential flowering occurs on Echium plantagineum in Australia, with the larvae of Thrips imaginis moving daily to a fresh flower (Kirk 1984). In Sarawak, various species of genus Thrips are considered pollinators of Popowia pisocarpa (Momose et al 1998). Notwithstanding, information is frequently missing on one or more events in the sequence diagramed here.In addition to recorded specialized systems, there are many poorly known systems wherein thrips are moderate to low-level co-pollinators. Thrips adults bearing pollen grains breed in the flowers of many plant families, and Old World Fabaceae often have species-specific thrips in their flowers. Pollination by thrips did not escape the keen eye of Charles Darwin (1892, p.11) who was frequently hindered in his pollination experiments, by thrips which “... no net will exclude”. Wind-pollination is commonly confused with thrips-pollination because netting rarely can exclude these insects, and plant breeders relying on hand pollination for specific crosses sometimes obtain unusual results due to pollen carried by thrips. Some thrips species are known only from particular hosts but the degree of thrips host specificity is often uncertain due to lack of detailed observations (Mound 2013).
Thrips bearing pollen grains attributable to either a ginkgoalean or cycad are reported from Early Cretaceous Spanish amber (Peñalver et al 2012), and pollination of gymnosperms by thrips could even date back to the Late Permian. Along with other insects, thrips are certainly very ancient pollinators (Frame 2003); and although they, like most pollinators, consume many pollen grains (Kirk 1987), it is unwise to dismiss them as mere pollen predators.
Darwin, C. (1892) The effects of cross and self fertilization in the vegetable kingdom. D. Appleton & Company, New York.
Fiala B, Meyer U, Hashim R & Maschwitz U (2011) Pollination systems in pioneer trees of the genus Macaranga (Euphorbiaceae) in Malaysian rainforests. Biological Journal of the Linnean Society 103: 935-953.
Frame D (2003) Generalist flowers, biodiversity and florivory: implications for angiosperm origins. Taxon 52: 681-685.
Hagerup E & Hagerup O (1953) Thrips pollination of Erica tetralix. New Phytologist 52: 1-7.
Kirk WD (1984) Ecological studies on Thrips imaginis Bagnall (Thysanoptera) in flowers of Echium plantagineum in Australia. Australian Journal of Ecology 9: 9-18.
Kirk WD (1987) How much pollen can thrips destroy? Ecological Entomology 12: 31-40.
Kirk WD (1997) Feeding. Pp. 65-118 in Lewis, T. (ed) Thrips as crop pests. CAB International, Oxon, UK
Momose K, Nagamitsu T & Inoue T. (1998) Thrips cross-pollination of Popowia pisocarpa (Annonaceae) in a lowland dipterocarp forest in Sarawak. Biotropica 30: 444-448.
Moog U, Fiala B, Federle W & Maschwitz U (2002) Thrips pollination of the dioecious ant plant Macaranga hullettii (Euphorbiaceae) in Southeast Asia. American Journal of Botany 89: 50-59.
Morgan HP (2007) Thrips as primary pollinators of sympatric species of Chamaedorea (Arecaceae) in Belize. Ph.D. Dissertation, City University of New York, New York.
Mound LA (2013) Homologies and host-plant specificity: recurrent problems in the study of thrips. Florida Entomologist 96(2): 318-322.
Mound LA & Terry I (2001) Thrips pollination of the central Australian cycad, Macrozamia macdonnellii (Cycadales). International Journal of Plant Science 162: 147-154.
Terry I, Moore CJ, Walter GH, Forster PI, Roemer RB, Donaldson JD & Machin PJ (2004) Association of cone thermogenesis and volatiles with pollinator specificity in Macrozamia cycads. Plant Systematics and Evolution 243: 233-247.
Peñalver E, Labandeira CC, Barrón E, Delclòs X, Nel P, Nel A, Tafforeau P & Soriano C (2012) Thrips pollination of Mesozoic gymnosperms. Proceedings of the National Academy of Sciences 109: 8623-8628.
Varatharajan R, Shyam Maisnam, Shimray CV & Rachana RR (2016) Pollination Potential of Thrips (Insecta:Thysanoptera) - An Overview. Zoo's Print 31(4): 6-12. http://www.zoosprint.org/ZooPrintMagazine/2016/April/6-12.pdf
Williams G, Adams P & Mound LA (2001) Thrips (Thysanoptera) pollination in Australian subtropical rainforests, with particular reference to pollination of Wilkiea huegeliana. (Monimiaceae). Journal of Natural History 35: 1-21
Zerega NJC, Mound LA & Weiblen GD (2004) Pollination in the New Guinea endemic Antiaropsis decipiens (Moraceae) is mediated by a new species of thrips, Thrips antiaropsidis sp. nov. (Thysanoptera: Thripidae). International Journal of Plant Science 165: 1017-1026.
Acknowledgements This work has benefited from an “ Investissement d’Avenir ” grant managed by Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01).