Palynivore

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Honeybee collecting pollen

In zoology, a palynivore /pəˈlɪnəvɔːɹ/, meaning “pollen eater” (from Greek παλύνω palunō, "strew, sprinkle", and Latin, vorare, meaning “to devour”) is an herbivorous animal which selectively eats the nutrient-rich pollen produced by angiosperms and gymnosperms. Most true palynivores are insects or mites. The category in its strictest application includes essentially all bees, and a few different kinds of wasps [1], as pollen is often the only solid food consumed by all life stages in these insects (palynivorous mites and thrips typically feed on the liquid content of the pollen grains without actually consuming the exine). The list is expanded greatly if one takes into consideration species where either the larval or adult stage feeds on pollen, but not both; there are other wasps which are in this category, as well as many beetles [2], flies, butterflies, and moths. One such example of a species that only consumes pollen in its larval stage is the Apis mellifera carnica[3] There is a vast array of different insects that will feed opportunistically on pollen, as will various birds, orb-weaving spiders[4] and other nectarivores.

Formed in the anther, or the male part of the flower, pollen is a male gametophyte[5]. Pollen is critical to fertilize the female part of the flower, and is a food source for palynivores. There is evidence that suggests palynivory dates back to at least the Permian period [6]. It is likely that a coevolution has occurred between plants and palynivores in a form of mutualism. This can be seen in the relative size of pollen, the ease by which pollen is accessible to palynivores, and the great effort by plants to advertise their pollen to pollinators [7].

Evolution

The earliest evidence of palynivory can be traced back to the Silurian and Early Devonian eras.[8] Fossil evidence from these periods suggests that early arthropods, with unspecialized mandibular mouthparts, engaged in spore-feeding behavior.[8] Palynivory, which is thought to have derived from early spore feeders, emerged much later during the Pennsylvanian era.[8] Much of the evidence relating to palynivory evolution has been linked to a change in the structure of mandibular mouthparts, allowing for easier pollen collection.[8] Such evidence can be found in Cleoptera (beetles), the most diverse group of palynivores, wherein species have developed mouthparts for pollen collection in addition to the evolution of early mandibular appendages into specialized structures assisting in pollen consumption.[8] Furthermore, the evolution of mouthparts involved in nectar uptake has contributed to the evolution of palynivore mouthparts.[8] The beginnings of structures involved in nectar uptake can be found in early, unrelated insect clades.[8] The evolution of these structures occurred in three distinct tracks: sponge-like labellum of flies and caddisflies, siphon structures in butterflies and moths, and glossa in wasps and bees.[9] The evolution of various structural and morphological adaptations of present-day palynivores has also been thought to have co-evolved with pollen grains.[10]

During the Late Pennsylvanian, the abundance and diversity of plant fossils implies increased specificity of palynivore behaviour and highlights the co-evolution of this behaviour with plant species at the time.[8] Based on the morphological features of fossil remnants of the era, early palynivores are hypothesised to have belonged to the diaphanopterodean, protorthopteran, and hemipteroid taxonomic groups.[11] [12][13] Following this period, evolution and more specialized adaptations in palynivore mouthparts and pollen or prepollen found in the gut of fossilized insects showed convergence into three major lineages: Orthoptera, Coleoptera, Diptera, and Hymenoptera.[8] Currently, palynivores exist in 5 insect orders, Coleoptera, Diptera, Thysanoptera, Hymenoptera, and Lepidoptera, that are thought to have come about during the early Mesozoic period.[8]

Adaptations of Palynivores

Bees
Bees, part of the superfamily Apoidea, engage in palynivory extensively, especially in providing pollen for their offspring[14][15]. To effectively collect, transport, and consume pollen, bees have evolved specialized morphological and behavioral traits. To forage for pollen, bees must first find sources of pollen, which they do so through chemical, visual, and tactile signals given by flowers[15]. They collect from the flowers themselves with specialized hairs and, after storing the pollen gathered together with nectar, transport the pollen with evolved scopal or corbicular constructions on their bodies[15]. Bees have also evolved behavioral adaptations that involve some form of learning[15]. Most bees are also either oligolectic or polylectic, in which their foraging pattern overlap significantly closely during the day and/or seasonally to the bloom periods of flowers[15]. After their return to the nest, bees will communicate the locations of good foraging patches to other worker bees in a process called a waggle dance[16]. Most flowering plants benefit from the pollination that occurs while bees collect and transport pollen[17]. Bees often favor certain foraging patches[15], and while evidence shows that bumble bees for instance are flexible in their foraging patterns, deciding on different types of flowers based on the pollen’s protein:lipid ratios[17], these patterns directly influence the genetics of the flowering plant populations around them[15].
Ants
Ants, as part of the order Hymenoptera, are related to bees and similarly forage outside of their nests to transport protein back for their offspring[18]. While pollen is not the sole or primary food source, evidence from studies done on ants species in genii such as Zacrpytocerus, Cephalotes, Camponotus, Crematogaster, and Odontomachus show that pollen is consumed opportunistically and as a target in their diet[19][18]. In foraging, ants cannot fly to flowers to take pollen directly[18]. Instead, they collect it from places where pollen has fallen or the wind has carried pollen to[19]. Ants commonly store liquid food in their foregut and later regurgitate it to feed their offspring in the home nest [18]. Several species of neotropical ants, Cephalotini ants for example, collect pollen from leaves and store it in their bodies to later regurgitate[18]. However, during this process, they produce compressed masses of pollen called pellets, “infrabuccal pellets” in Cephalotini and first thought to be a mechanism for conserving water, that allow for greater efficiency in transporting pollen[18]. After ant offspring or worker ants consume the nutrient-rich parts of the pollen from these pellets, the membranes of pollen, unable to be digested, are then discarded[18].

Effects of Global Climate Change and the Future of Palynivores

It has been shown that the recent decrease in palynivores has led to a parallel decline in the plant species that rely on these pollinators [20]. These palynivores are essential to spreading the genes of these pollen producing plants and providing genetic diversity for these plants. While wind and other natural resources can help with this process of spreading pollen, they are not as specific not do they provide as direct a service as palynivores. As stated by Potts et al, a range of different environmental and climate changes such as the loss of habitat, the introduction of different agrochemicals, and global warming are projected to lead to the decrease in pollinator/ palynivore populations and consequently a decrease in pollination services [21]. While not much research has been conducted on palynivores in the wild, the bumble bee has been the most widely documented and there has shown evidence of population decline within both Belgium and the UK with 6 of the 16 non-parasitic bumble bees showing considerable decline and 4 showing possible signs of decline [21]. These observational studies have also shown that this decline has been similarly been mirrored in the populations of wild plants with which these bees are correlated [21]. However, this decline has not been prevalent among all populations of bumblebees. While many populations of bumblebees have shown a decline, there have been others that have stayed constant or even increased. In the same study of 16 non-parasitic bumble bees there were 6 populations that stayed constant or even increased over the course of the study [21].

The results from this bumblebee study can likewise be generalized for most palynivores. palynivores can generally be grouped in 2 categories: specific and general [20]. Specific palynivores are specialized to specific genus or species of plants while general palynivores can pollinate a wide range of plants. Because of the specialty of certain types of honey bees, their life cycles have adapted to be closely correlated with certain species of plants. However, when the pollination and flowering periods of these plants change because of different seasonal variations caused by climate change, the palynivore lifecycles are no longer in synch with that of the plant thereby causing a decline in both populations [21] [20]. However, this decline in specific palynivores can also lead to an increase in populations of general palynivores due to a decrease in competition and the increase in availability of resources.

Future Actions to Protect Palynivores

But even so, there has been a general decline in plant and palynivore species diversity which is predicted to continue with the current environmental trends seen in the release of greenhouse gasses and climate change. Given the extent of current research and evidence depicting the correlation between palynivore decline and a decline in pollinating plants reproductive success, it is important for individuals to take action to mitigate the loss of these species.

  1. Restore and protect palynivore habitat by identifying floral reserves of threatened migratory palynivores [22]
  2. Planting more native plants to attract local native palynivores
  3. Increasing the available habitat for palynivores in and around croplands and gardens [22]
  4. Mitigating the use of pesticides, agrochemicals, and herbicides [21]

References

  1. ^ Hunt, J H, Brown, P A, Sago, K M, and Kerker, J A (Apr. 1991). “Vespid Wasps Eat Pollen (Hymenoptera: Vespidae)”. Journal of the Kansas Entomological Society. 64(2): 127-130. .
  2. ^ Samuelson, G A (1994). “ Pollen Consumption and Digestion by Leaf Beetles” in Novel aspects of the biology of Chrysomelidae. Series Entomologica, 50. https://doi.org/10.1007/978-94-011-1781-4_10, .
  3. ^ Szolderits, M J, Crailsheim, K (1993). “A Comparison of Pollen Consumption and Digestion in Honeybee (Apis mellifera carnica) Drones and Workers.” Journal of Insect Physiology, 39(10): 877-881. doi:10.1016/0022-1910(93)90120-g, .
  4. ^ Eggs B, Sanders D (2013) Herbivory in Spiders: The Importance of Pollen for Orb-Weavers. PLoS ONE 8(11): e82637. doi:10.1371/journal.pone.0082637, .
  5. ^ McCormick S (2013) Pollen. Current Biology 23(22): R988-90. doi:10.1016/J.CUB.2013.08.016.
  6. ^ Krassilov V A, Rasnitsyn A P, Afonin S A (2007) Pollen eaters and pollen morphology: co-evolution through the Permian and Mesozoic. African Invertebrates 48(1): 3-11. .
  7. ^ Labandeira, C C (2000) The Paleobiology of Pollination and Its Precursors. Paleontological Society Papers 6: 233-269. .
  8. ^ a b c d e f g h i j Labandeira, C.C. (2000). “The Paleobiology of Pollination and Its Precursors.” Paleontological Society Papers,6: 233-269. https://repository.si.edu/bitstream/handle/10088/5961/Paleont_Soc_Papers_2000.pdf.
  9. ^ Smith, J.J.B (1985). "Feeding mechanisms". In G.A. Kerkut and L.E. Gilbert (eds.), Comprehensive Insect Physiology, Biochemistry, and Pharmacology, Volume 4. Oxford University Press, Oxford, U.K. pp. 33-85.
  10. ^ Krassilov, V.A., Rasnitsyn A.P., Afonin S.A. (Apr. 2007). “Pollen eaters and pollen morphology: co-evolution through the Permian and Mesozoic.” African Invertebrates, 48(1): 3-11.
  11. ^ Richardson, E.S., JR. (1980). "Life at Mazon Creek". In R.L. Langenheim, Jr. and C.J. Mann, (eds.), Middle and Late Pennsylvanian Strata of [the] Margin of [the] Illinois Basin. University of Illinois Press, Urbana, IL. pp. 217-224.
  12. ^ Scott, A.C., Taylor, T.N.. (1983). "Plant/animal interactions during the Upper Carboniferous". Botanical Review, 49: 259-307.
  13. ^ Kukalová-Peck, J. (1987). "New Carboniferous Diplura, Monura, Thysanura, the hexapod ground plan, and the role of thoracic side lobes in the origin of wings (Insecta)". Canadian Journal of Zoology, 65: 2327-2345.
  14. ^ Szolderits, M. J., Crailsheim, K. (1993). “A Comparison of Pollen Consumption and Digestion in Honeybee (Apis mellifera carnica) Drones and Workers.” Journal of Insect Physiology, 39(10): 877-881. doi:10.1016/0022-1910(93)90120-g
  15. ^ a b c d e f g Thorp, R. (1979). “Structural, Behavioral, and Physiological Adaptations of Bees (Apoidea) for Collecting Pollen”. JSTOR. 66(4): 788-812.
  16. ^ Wario, Fernando & Wild, Benjamin & Rojas, Raúl & Landgraf, Tim. (2017). Automatic detection and decoding of honey bee waggle dances. PLOS ONE. 12. doi:10.1371/journal.pone.0188626.
  17. ^ a b Vaudo, A.D., Patch, H.M., Mortensen, D.A., Tooker, J.F., and Grozinger, C.M. (Jul. 2016). “Macronutrient rations in pollen shape bumble bee (Bombus impatiens)foraging strategies and floral preferenecs.” PNAS, 113(28): E4035-E4042.
  18. ^ a b c d e f g Baroni, C. (April. 1997). “Pollen Eating, Storing, and Spitting by Ants”. Springer-Verlag. Naturwissenschaften 84: 256–258.
  19. ^ a b Cembrowski, A. R., Reurink, G., Hernandez, L. A., Sanders, J.G., Youngerman E., Frederickson, M. E. (Aug. 2015). “Sporadic Pollen Consumption Among Tropical Ants.” Insects Sociaux, 62(3): 379-82. doi:10.1007/s00040-015-0402-x.
  20. ^ a b c Thomann, M, Imbert, E, Devaux, C, & Cheptou, P (2013) Flowering plants under global pollinator decline. Trends in Plant Science 18(7):353-359. doi:10.1016/j.tplants.2013.04.002. .
  21. ^ a b c d e f Potts, S (2010) Global Pollinator Declines: Trends, Impacts, and Drivers. Cell Press 25(6):345-353. .
  22. ^ a b The Potential Consequences of Pollinator Declines on the Conservation of Biodiversity and Stability of Food Crop Yields. Conservation Biology 12(1): 8-17. doi:10.1111/j.1523-1739.1998.97154.x. .
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