Polistes semenowi

Last updated

Polistes semenowi
Polistes semenowi (10.3897-zookeys.713.11335) Figure 57.jpg
Female
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Hymenoptera
Family: Vespidae
Subfamily: Polistinae
Tribe: Polistini
Genus: Polistes
Species:
P. semenowi
Binomial name
Polistes semenowi
Morawitz, 1889
Synonyms [1]
  • Polistes semenowiiDalla Torre, 1894 (Missp.)
  • Polistes sulciferZimmermann, 1930
  • Pseudopolistes semenoviWeyrauch, 1937 (Missp.)
  • Pseudpolistes sulcifer v. similatorZirngiebl, 1955

Polistes semenowi is a species of paper wasp in the genus Polistes that is found in southeastern and southern central Europe, as well as central Asia, and was until 2017 erroneously known by the name Polistes sulcifer, while a different species was incorrectly believed to represent P. semenowi (this species has been named Polistes austroccidentalis since 2017). [1] [2] [3] [4] It is one of only four known Polistes obligate social parasites, sometimes referred to as "cuckoo paper wasps", [5] and its host is the congeneric species Polistes dominula . [6] As an obligate social parasite, this species has lost the ability to build nests, and relies on the host workers to raise its brood. [7] P. semenowi females use brute force, followed by chemical mimicry in order to successfully usurp a host nest and take over as the queen. [7] [8]

Contents

Taxonomy and phylogeny

Polistes is the only genus in the tribe Polistini of the subfamily Polistinae. [9] Species in this subfamily are one of several lineages often known as paper wasps. [10] Polistes semenowi, first named by Morawitz in 1889, is a member of the monophyletic species group once known as Sulcopolistes , [11] [12] which contains only four species (the others being Polistes atrimandibularis , Polistes austroccidentalis , and Polistes maroccanus ), [1] all of them obligate social parasites on other Polistes species. [6] Sulcopolistes was mistakenly thought to be an entirely different genus but was incorporated into the subgenus Polistes by Carpenter in 1991. Additionally, this species group is phylogenetically close to Polistes dominula, the only host species of P. semenowi. [12]

Description

Polistes semenowi, like most other paper wasps, are typically 0.7–1.0 inches long. [10] Because it is a social parasite, it is adapted for fighting off the host species, and has some morphological distinctions. [6] P. semenowi is known to have larger mandibles and anterior legs than those of related species. [2] It also has a more square-shaped head, which is hypothesized to have evolved from the need for robust muscles to power the larger mandibles. Additionally, there is often a black band in the lower half of the clypeus. This trait in particular distinguishes it from its host species P. dominula. [13] P. semenowi males typically have a more complete coloration of the body than the females, with the colors ranging from yellow to almost white. [4]

A typical paper wasp nest resembles a papery material, and is made of saliva and fibers from wood and plants. [10] P. semenowi, however, has lost the nest making ability. [3] Instead, it relies on the nests of its host species Polistes dominula , whose nests are made of the typical paper material with many combs.

Distribution

P. semenowi is found in southeastern and south-central Europe, as well as central Asia. [1]

Colony cycle

Nest of the yellow paper wasp, P. dominula, host to the cuckoo wasp Yellow Paper Wasp.jpg
Nest of the yellow paper wasp, P. dominula , host to the cuckoo wasp

P. semenowi is a permanent workerless species, and consists only of reproductive males and females. [6] [14] Because P. semenowi is an obligate social parasite, its cycle depends heavily on that of its host species P. dominula, also known as the yellow paper wasp. As mentioned previously, P. semenowi queens (mated females) overwinter at high altitudes. [2] Come May, they emerge. They tend to overwinter for a longer period of time than their host P. dominula, which emerges in April. [2] This ensures that the parasites reach the host nest at the optimal time: just before worker emergence, when only the host foundresses are in the nest, leading to an easier invasion. [5] Once a queen P. semenowi has successfully invaded a nest, the host nest is built up by the host workers after their emergence in early summer. P. semenowi has an annual cycle, and it has been shown that parasitic members only stay in the host nests for around 50 days. [7] After emergence of the P. semenowi reproductive individuals, mating occurs, and fertilized females overwinter while males die off.

Brood parasite

P. semenowi is an obligate social parasite. Even more specifically, it is a brood parasite. This means that they lay their eggs in the nests of other species and influence the host into providing the parental care for their young. [15] The cuckoo (bird) is the most familiar example of a brood parasite, hence P. semenowi's common name, the cuckoo wasp.

P. semenowi has lost the ability to take care of its own young, [7] so if an overwintering female fails to find a host nest to usurp, she leaves no offspring. A successful female relies on the host workers to care for her brood. The parasite brood develop from eggs to adults more quickly than the host brood, 25 days vs. 33 days respectively. [2] Based on behavioral observations, host workers tended to visit parasite young much more frequently than host young, and each parasitic larva was visited much more often by a host worker than by its own mother. Surprisingly, it is not the parasite queen who is controlling this phenomenon, but it is the parasite larva that are somehow able to attract unrelated host workers on their own. One hypothesis is that the larva have 'hungry signs', much like in cuckoo birds, that manipulate the host workers into thinking they are still hungry. [2] Since food supply during the larval stage dictates which caste a wasp will become, [16] this manipulation of host workers is essential to P. semenowi because all larvae need to emerge as reproductives. [2]

Usurpation

In order for P. semenowi to have offspring, it must invade the nest of its host and exploit its colony. This invasion of a colony is called usurpation, and it is done in a very systematic way. After a long hibernation, the overwintering females, all fertilized queens, search for a host nest. The females emerge from overwintering relatively late, which allows them to look for a host colony before worker emergence, when there are only foundresses present in the nest. This allows for the simplest usurpation. When a suitable host nest is found, the female initially uses brute force to fight the host foundress and gain control of the nest. The outcome of these fights is often predicted by the relative body size of the two females. [8] Most often, the host foundress is evicted or killed. [7] Once inside the host nest, the P. semenowi female undergoes the process of changing her cuticular hydrocarbons to match that of the host colonies (more information on cuticular hydrocarbons can be found in the camouflage section). This helps the parasitic queen remain accepted by the host colony. The parasitic queen now controls the nest, and can lay her eggs. The host workers continue on as normal, raising both the host and parasite brood. [2]

Restlessness and hyperkinesis

Usurpation is only successful when done within a very specific seasonal time window, before emergence of the host workers. During this time window, a phenomenon has been observed that is called 'usurpation restlessness'. This is when a wasp's activity level increases during the ideal usurpation window, theoretically making usurpation easier. This increased activity level is shown even in the lab setting. [3] In addition to usurpation restlessness, which occurs seasonally, P. semenowi females show hyperkinesis, or extra activity, in the middle of each day. This is thought to have evolved so the parasitic females are able to perform nest usurpations in the middle of the day, when the host species is out foraging, and so defense of the nest is lower. [7]

Behavior

Dominance hierarchy

The only known host of P. semenowi is P. dominula, a species that will often have multiple foundresses. [7] If this is the case, then there is a dominance hierarchy present. There will be one dominant female, also known as the queen or alpha female, and one or more subordinate, or beta females. The dominant female spends her time laying eggs and interacting socially, while the subordinate females act much more like workers, spending time taking care of the brood and foraging. [17] The dominant female is in charge of all of the workers. When the P. semenowi female enters the host nest for usurpation, she aggressively fights with the alpha P. dominula. If the usurpation is successful, the alpha P. dominula loses its dominant position, and is replaced by the P. semenowi female. The new female now adopts the chemical signature of the previous alpha and takes over all her previous duties. She is now the queen of the nest. [7]

Reproductive suppression

As queen, the P. semenowi female is the only one allowed to lay eggs. Dapporto et al. hypothesized that the queen suppresses the reproductive capabilities of the other females using chemical signaling. [7] If the alpha female is removed for any reason, the next subordinate female will take over her role as the reproductive. This is why the chemical mimicry of the P. dominula alpha females cuticular hydrocarbons is so important. Without matching the signal, the P. semenowi female will lose reproductive rights and will be unable to exploit the host's resources for its own reproduction, its ultimate goal as an obligate social parasite. Parasite females are unable to suppress subordinate reproduction completely. In comparison with unparasitized control nests, subordinate females under a parasite queens laid more eggs. [18] This may suggest that P. dominula subordinate females are evolving a way to resist the parasitic females efforts. [18]

Division of labor

Instead of labor being divided up within members of its own species, P. semenowi gives most of its labor to its host species. P. semenowi is a permanently workerless species, and cannot take care of its own brood, and so relies on P. dominula workers to do this for them. [7] This work involves building up the nest, foraging, and feeding the young. Because P. semenowi consists only of reproductive males and females, [14] the fertile reproductive female's main job is to successfully usurp a nest in order to raise her brood, while the reproductive male's primary job is to fertilize the reproductive females.

Camouflage and mimicry

After a P. semenowi female has taken over a host nest, it changes its proportions of cuticular hydrocarbons (chemicals on the surface of all insects that play a role in chemical communication) to match that of the host. [14] This is hypothesized to be done by two mechanisms. Camouflage is the term given to the process of acquiring the cuticular hydrocarbons directly from the host individuals or nest, while mimicry is the term given to describe the process where the hydrocarbons are produced by the parasite itself. [14] P. semenowi is hypothesized to use both methods during usurpation. Upon invasion of the host nest, P. semenowi queens are observed rapidly stroking their abdomen on the host nest. [14] This, along with grooming and licking of the host foundresses and workers, is thought to be the way that the P. semenowi queen camouflages herself in the host cuticular hydrocarbons. [14] Chemical mimicry is thought to occur due to the presence of an enlarged Van der Vecht's organ on the abdomen of P. semenowi queens. [19] This organ secretes chemicals involved in dominance recognition, and is thought to be enlarged in P. semenowi due to its need for quick chemical mimicry, before worker emergence. [19] It has been shown that a full host cuticular signature is developed within only 3 days of usurpation. [14]

Diet

P. semenowi larvae feed on what P. dominula feeds on, since it is the host workers who are collecting the food. It has been found that P. dominula food is from three insect orders. [20] P. dominula, unlike many other social wasps, is known as a very generalist predator, and is both opportunistic and very flexible in selecting their prey. [21] Adult P. semenowi wasps have been shown to eat the larvae of other insect species including Tenebrio molitor larvae (a beetle species) [2] and fly maggots. [7] It has also been shown that the parasitic P. semenowi female may use the host eggs as nutrition soon after usurpation occurs. [7] Additionally, in P. semenowi, a peculiar phenomenon is observed during usurpation season. The female is known to feed on flowers in the early morning and in the late afternoon. This is thought to have evolved so the female could attempt to usurp in the middle of the day, when the host is out feeding. [6]

Related Research Articles

<span class="mw-page-title-main">Paper wasp</span> Vespid wasps that gather fibers from dead wood and plant stems

Paper wasps are vespid wasps and typically refers to members of the vespid subfamily Polistinae, though it often colloquially includes members of the subfamilies Vespinae and Stenogastrinae, discussed elsewhere, which also make nests out of paper. Paper wasp nests are characterized by open combs with down pointing cells. Some types of paper wasps are also sometimes called umbrella wasps, due to the distinctive design of their nests.

<i>Polistes</i> Genus of wasps

Polistes is a cosmopolitan genus of paper wasps and the only genus in the tribe Polistini. Vernacular names for the genus include umbrella wasps, coined by Walter Ebeling in 1975 to distinguish it from other types of paper wasp, in reference to the form of their nests, and umbrella paper wasps. Polistes is the single largest genus within the family Vespidae, with over 200 recognized species. Their innate preferences for nest-building sites leads them to commonly build nests on human habitation, where they can be very unwelcome; although generally not aggressive, they can be provoked into defending their nests. All species are predatory, and they may consume large numbers of caterpillars, in which respect they are generally considered beneficial.

<span class="mw-page-title-main">Brood parasitism</span> Animal reliance on other individuals to raise its young

Brood parasitism is a subclass of parasitism and phenomenon and behavioural pattern of certain animals, brood parasites, that rely on others to raise their young. The strategy appears among birds, insects and fish. The brood parasite manipulates a host, either of the same or of another species, to raise its young as if it were its own, usually using egg mimicry, with eggs that resemble the host's.

An obligate parasite or holoparasite is a parasitic organism that cannot complete its life-cycle without exploiting a suitable host. If an obligate parasite cannot obtain a host it will fail to reproduce. This is opposed to a facultative parasite, which can act as a parasite but does not rely on its host to continue its life-cycle. Obligate parasites have evolved a variety of parasitic strategies to exploit their hosts. Holoparasites and some hemiparasites are obligate.

<span class="mw-page-title-main">Polistinae</span> Subfamily of insects

The Polistinae is a subfamily of eusocial wasps belonging to the family Vespidae. They are closely related to the wasps and true hornets of the subfamily Vespinae, containing four tribes. With about 1,100 species total, it is the second-most diverse subfamily within the Vespidae, and while most species are tropical or subtropical, they include some of the most frequently encountered large wasps in temperate regions.

<span class="mw-page-title-main">European paper wasp</span> Species of wasp

The European paper wasp is one of the most common and well-known species of social wasps in the genus Polistes. Its diet is more diverse than those of most Polistes species—many genera of insects versus mainly caterpillars in other Polistes—giving it superior survivability compared to other wasp species during a shortage of resources.

<i>Polistes gallicus</i> Species of wasp

Polistes gallicus is a species of paper wasp found in various parts of Europe, excluding England, Denmark, and Scandinavia, from warmer climates to cooler regions north of the Alps. Nests of these social insects are created in these various conditions. The Polistes species use an oral secretion to construct their nests, which consist of a combination of saliva and chewed plant fibers. This structural mixture physically protects the nest from various harsh elements and from weathering over time.

<i>Polistes annularis</i> Species of wasp

Polistes annularis is a species of paper wasp found throughout the eastern half of the United States. This species of red paper wasp is known for its large size and its red-and-black coloration and is variably referred to as a ringed paper wasp or jack Spaniard wasp. It builds its nest under overhangs near bodies of water that minimize the amount of sunlight penetration. It clusters its nests together in large aggregations, and consumes nectar and other insects. Its principal predator is the ant, although birds are also known to prey on it. Unlike other wasps, P. annularis is relatively robust in winter conditions, and has also been observed to store honey in advance of hibernation. This species has also been used as a model species to demonstrate the ability to use microsatellite markers in maternity assignment of social insects.

<i>Polistes metricus</i> Species of wasp

Polistes metricus is a wasp native to North America. In the United States, it ranges throughout the southern Midwest, the South, and as far northeast as New York, but has recently been spotted in southwest Ontario. A single female specimen has also been reported from Dryden, Maine. Polistes metricus is dark colored, with yellow tarsi and black tibia. Nests of Polistes metricus can be found attached to the sides of buildings, trees, and shrubbery.

<i>Polistes fuscatus</i> Species of insect

Polistes fuscatus, whose common name is the dark or northern paper wasp, is widely found in eastern North America, from southern Canada through the southern United States. It often nests around human development. However, it greatly prefers areas in which wood is readily available for use as nest material, therefore they are also found near and in woodlands and savannas. P. fuscatus is a social wasp that is part of a complex society based around a single dominant foundress along with other cofoundresses and a dominance hierarchy.

<i>Polistes nimpha</i> Species of wasp

Polistes nimpha is a eusocial paper wasp found all over Europe, with particular sightings in Turkey, Finland, Estonia, and Latvia. It is also found in northern Africa, Pakistan, Iran, India, Kazakhstan, Mongolia, and China. The climate in these areas is relatively cold and snowy in the winter, while summers are usually hot and dry, with steppe vegetation. Polistes nimpha colonies are relatively small and easily manipulated.

<i>Polistes atrimandibularis</i> Species of wasp

Polistes atrimandibularis is one of four obligate social parasites among the Polistes wasps found in Europe. Of the four social paper wasp parasite species known, it is the smallest. It parasitizes multiple species such as P. dominula, P. nimpha, P. associus, P. gallicus, and P. biglumis. Females of P. atrimandibularis are unable to build a nest or produce workers, and therefore rely entirely on the host colony.

<i>Polistes austroccidentalis</i> Species of wasp

Polistes austroccidentalis is a kleptoparasitic paper wasp that is found in several regions of high altitude in Europe, and until 2017 was universally mistakenly referred to as Polistes semenowi, which is instead the correct name of the species formerly known as "Polistes sulcifer". As one of only four obligate parasites in the subgenus Polistes, it uses the nests of other paper wasps to rear its young. To evade detection by the host nest, P. austroccidentalis employs mimicry by adjusting its cuticular hydrocarbons to match those of the host. Once the host nest has been infiltrated, the parasitic female physically attacks the host queen to subdue her and become the colony's new queen. P. austroccidentalis displays several morphological adaptations for parasitism such as increased mandible size and an enlarged Van der Vecht's organ. This species is unusual because it does not have the ability to produce workers and is only able to produce individuals who have the capacity to reproduce.

<i>Polistes biglumis</i> Species of wasp

Polistes biglumis is a species of social wasp within Polistes, the most common genus of paper wasp. It is distinguished mainly by its tendency to reside in montane climates in meadows or alpine areas. Selection pressure from the wasp's environment has led to several idiosyncrasies of its behavior and lifecycle with respect to its relative species in the genus Polistes. It alone among paper wasps is often polyandrous. In addition, it has a truncated nesting season that gives rise to unique competitive dynamics among females of the species. P. biglumis wasps use an odor-based recognition system that is the basis for all wasp-to-wasp interaction of the species. The wasp's lifecycle is highly intertwined with that of Polistes atrimandibularis, an obligate social parasite wasp that frequently invades the combs of P. biglumis wasps.

<i>Polistes dorsalis</i> Species of wasp

Polistes dorsalis is a species of social wasps that can be found throughout various parts of North America. It is classified under the Vespidae within the genus of Polistes. Male Polistes dorsalis wasps can be distinguished from other Polistes species by their distinctly prominent median tubercle of sternum 7. Both sexes can also be recognized due to their v- shaped yellow markings on their head. They are distributed widely across North America and can be found in sheltered nests, typically closer to the ground. These wasps live in a dominance hierarchy in which the queen's role differs from that of ordinary workers. When threatened, these wasps can deliver moderately painful stings. Their venom might also be of human interest for their antimicrobial uses.

Polistes erythrocephalus is a species of paper wasp in the subfamily Polistinae of family Vespidae found in Central and South America. P. erythrocephalus is a eusocial wasp, meaning that it possesses both reproductive and non-reproductive castes. The cooperation between the two castes to raise young demonstrates the altruistic nature of these wasps. P. erythrocephalus exhibits a four-stage colony cycle, as do many other Polistes wasps. This species generally feeds on larvae, occasionally their own, and is preyed upon by species such as army ants.

The name cuckoo paper wasp refers to a monophyletic species group of brood-parasitic paper wasps in the genus Polistes. This species group contains only four species; Polistes atrimandibularis, P. austroccidentalis, P. maroccanus, and P. semenowi, all of them obligate social parasites of other Polistes species.

<span class="mw-page-title-main">Nest usurpation</span>

Nest usurpation is when the queen of one species of eusocial insects takes over the colony of another species.

<i>Vespula infernalis</i> Species of wasp

Vespula infernalis is an obligate parasitic wasp, parasitizing the nests of other species in the genus Vespula. Its common host species is V. acadica in North America. It is sometimes called the cuckoo yellowjacket wasp due to its inquiline lifestyle. They differ from other parasitic wasps in their intensely aggressive behaviour during invasion and occupation of the host colony. Several morphological adaptations such as bigger body parts and highly curved stingers are present in these wasps to aid their aggressive parasitic behaviour.

Van der Vecht's gland or Van der Vecht's organ is a gland which is located in an area of modified cuticle on the rearmost gastral sternite of female wasps. This gland secretes chemicals which are important in the determination and maintenance of the hierarchy of groups of eusocial wasps and are used in the defence of the nests in others. In the Asian giant hornet the Van der Vecht's gland is used to scent mark hives of honey bees to attract other members of their colony to cooperatively attack the hive; the only known case of the gland's use to scent mark a food source. In the cleptoparasitic paper wasp Polistes semenowi the female usurps the host foundress, usually Polistes dominula and uses an enlarged Van der Vecht's gland to produce large quantities of hydrocarbons and to control the host workers, and even sometimes the host foundress. The gland was discovered by, and named in honour of, the Dutch entomologist Jacobus van der Vecht.

References

  1. 1 2 3 4 Schmid-Egger C, van Achterberg K, Neumeyer R, Morinière J, Schmidt S (2017) Revision of the West Palaearctic Polistes Latreille, with the descriptions of two species – an integrative approach using morphology and DNA barcodes (Hymenoptera, Vespidae). ZooKeys 713: 53-112. https://doi.org/10.3897/zookeys.713.11335
  2. 1 2 3 4 5 6 7 8 9 Cervo, R; Macinai, V; Dechigi, F; Turillazzi, S (2004). "Fast growth of immature brood in a social parasite wasp: a convergent evolution between avian and insect cuckoos". American Naturalist. 164 (6): 814–820. doi:10.1086/425987. PMID   29641918. S2CID   4805590.
  3. 1 2 3 Ortolani, I; Turillazzi, S; Cervo, R (2008). "Spring usurpation restlessness: a wasp social parasite adapts its seasonal activity to the host cycle". Ethology. 114 (8): 782–788. Bibcode:2008Ethol.114..782O. doi:10.1111/j.1439-0310.2008.01525.x.
  4. 1 2 Polasek, O. (2000). "Notes on Polistes sulcifer ZIMMERMANN 1930 in Croatia (Hymenoptera, Vespidae)". Linzer Biol. Beitr. 32 (2): 1063–1070.
  5. 1 2 Cervo, R.; Turillazzi, S. (1996). "Host nest preference and nest choice in the cuckoo paper wasp Polistes sulcifer (Hymenoptera, Vespidae)"". J. Insect Behav. 9 (2): 297–306. Bibcode:1996JIBeh...9..297C. doi:10.1007/bf02213872. S2CID   25346162.
  6. 1 2 3 4 5 Ortolani, I.; Cervo, R. (2009). "Coevolution of daily activity timing in a host-parasite system". Biological Journal of the Linnean Society. 96 (2): 399–405. doi: 10.1111/j.1095-8312.2008.01139.x .
  7. 1 2 3 4 5 6 7 8 9 10 11 12 Dapporto, L; Cervo, R; Sledge, MF; Turillazzi, S (2004). "Rank integration in dominance hierarchies of host colonies by the paper wasp social parasite Polistes sulcifer (Hymenoptera, Vespidae)". J Insect Physiol. 50 (2–3): 217–223. doi:10.1016/j.jinsphys.2003.11.012. PMID   15019524.
  8. 1 2 Cini, A; Bruschini, C; Poggi, L; Cervo, R (2011). "Fight or fool? Physical strength, instead of sensory deception, matters in host nest invasion by a wasp social parasite". Anim Behav. 81 (6): 1139–1145. doi:10.1016/j.anbehav.2011.02.017. S2CID   53179330.
  9. ↑ "Polistes." Wikipedia. Wikimedia Foundation, 2010. Web. 24 Sept. 2014.
  10. 1 2 3 "Paper Wasp" Microsoft Encarta Online Encyclopedia 2006.
  11. ↑ Carpenter, James M. "Phylogeny and Biogeography of Polistes." Natural History and Evolution of Paper-wasps. Ed. Stefano Turillazzi and Mary Jane. West-Eberhard. Oxford: Oxford UP, 1996. 18-57. Print.
  12. 1 2 Choudary, M; Strassmann, JE; Queller, DC; Turillazzi, S; Cervo, R (1994). "Social parasites in polistine wasps are monophyletic: implications for sympatric speciation". Proceedings of the Royal Society of London B: Biological Sciences. 257 (1348): 31–35. doi:10.1098/rspb.1994.0090. S2CID   86279569.
  13. ↑ Ortolani, I; Zecchini, L; Turillazzi, S; Cervo, R (2010). "Recognition of a paper wasp social parasite by its host: evidence for a visual signal reducing host aggressiveness". Anim Behav. 80 (4): 683–688. doi:10.1016/j.anbehav.2010.07.003. S2CID   53199391.
  14. 1 2 3 4 5 6 7 Sledge, M.F.; Dani, F.R.; Cervo, R.; Dapporto, L.; Turillazzi, S. (2001). "Recognition of social parasites as nestmates: adoption of colony-specific host cuticular odours by the paper wasp parasite Polistes sulcifer". Proceedings of the Royal Society of London B. 268 (1482): 2253–2260. doi:10.1098/rspb.2001.1799. PMC   1088873 . PMID   11674873.
  15. ↑ Davies, Nicholas; Krebs, John; West, Stuart (1993). An Introduction to Behavioural Ecology (4th ed.). Oxford: Wiley-Blackwell. p. 249. ISBN   978-1-4051-1416-5.
  16. ↑ O'Donnell, S (1998). "Reproductive caste determination in eusocial wasps (Hymenoptera: Vespidae)" (PDF). Annual Review of Entomology. 43: 323–346. doi:10.1146/annurev.ento.43.1.323. PMID   15012393.
  17. ↑ Theraulaz, G.; Pratte, M.; Gervet, J. (1989). "Effects of removal of alpha individuals from a Polistes dominulus Christ wasp society: Changes in behavioural patterns resulting from hierarchical changes". Actes Coll. Insectes Soc. 5: 169–179.
  18. 1 2 Cini, Alessandro; Nieri, Rachele; Dapporto, Leonardo; Monnin, Thibaud; Cervo, Rita (2014). "Almost royal: incomplete suppression of host worker ovarian development by a social parasite wasp". Behav Ecol Sociobiol. 68 (3): 467–475. doi:10.1007/s00265-013-1661-z. S2CID   253807610.
  19. 1 2 Petrocelli, Iacopo; Turillazzi, Stefano (2013). "Comparative morphology of Van der Vecht's organ in Polistes social parasties: host ecology and adaptation or the parasite". Biological Journal of the Linnean Society. 109 (2): 313–319. doi: 10.1111/bij.12053 .
  20. ↑ Nonacs, Peter; Reeve, Hudson (1993). "Opportunistic adoption of orphaned nests in paper wasps as an alternative reproductive strategy". Behavioural Processes. 30: 47–60. doi:10.1016/0376-6357(93)90011-f. PMID   24896471. S2CID   25676710.
  21. ↑ Cervo, R.; Zacchi, F.; Turillazzi, S. (2000). "Polistes dominulus (Hymenoptera, Vespidae) Invading North America: Some Hypotheses for Its Rapid Spread". Insectes Sociaux. 47 (2): 155–157. doi:10.1007/pl00001694. S2CID   45652070.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.