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Brood parasitism

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A shiny cowbird chick (left) being fed by a rufous-collared sparrow
Eastern phoebe nest with one brown-headed cowbird egg (at bottom left)
Shiny cowbird parasiting Masked water Tyrant in Brazil

Brood parasites are organisms 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, using brood mimicry, for example by having eggs that resemble the host's (egg mimicry).

Brood parasitism relieves the parasitic parents from the investment of rearing young or building nests for the young, enabling them to spend more time on other activities such as foraging and producing further offspring. Bird parasite species mitigate the risk of egg loss by distributing eggs amongst a number of different hosts.[1] As this behaviour damages the host, it often results in an evolutionary arms race between parasite and host as the pair of species coevolve.[2][3]

The strength of defenses and counter-adaptation rely on the host/parasitic species' ability to evolve; some host species have very strong rejection defenses resulting in the parasitic species evolving to have very close mimicry. In other species, hosts do not show rejection defenses and as a result, the parasitic species will show no evolved trait (example: egg mimicry).[4]

Birds

The goldeneye often lays its eggs in the nests of other females.
Further information: List of brood parasitic passerines

In many monogamous bird species, there are extra-pair matings resulting in males outside the pair bond siring offspring and used by males to escape from the parental investment in raising their offspring.[5] This form of cuckoldry is taken a step further when females of the goldeneye (Bucephala clangula) often lay their eggs in the nests of other individuals. Intraspecific brood parasitism is seen in a number of duck species, where females often lay their eggs in the nests of others.[6]

A Eurasian reed warbler raising a common cuckoo.
A black-collared starling feeding an Asian koel.

Interspecific brood-parasites include the indigobirds, whydahs, and honeyguides in Africa, cowbirds, Old World cuckoos, black-headed ducks, and some New World cuckoos in the Americas. Seven independent origins of obligate interspecific brood parasitism in birds have been proposed. While there is still some controversy over when and how many origins of interspecific brood parasitism have occurred, recent phylogenetic analyses suggest two origins in Passeriformes (once in New World cowbirds: Icteridae, and once in African Finches: Viduidae); three origins in Old World and New World cuckoos (once in Cuculinae, Phaenicophaeinae, and in Neomorphinae-Crotophaginae); a single origin in Old World honeyguides (Indicatoridae); and in a single species of waterfowl, the black-headed duck (Heteronetta atricapilla).[7][8][9]

Most avian brood parasites are specialists which parasitize only a single host species or a small group of closely related host species, but four out of the five parasitic cowbirds (all except the screaming cowbird) are generalists which parasitize a wide variety of hosts; the brown-headed cowbird has 221 known hosts. They usually lay only one egg per nest, although in some cases, particularly the cowbirds, several females may use the same host nest.[citation needed]

The common cuckoo presents an interesting case in which the species as a whole parasitizes a wide variety of hosts, including the reed warbler and dunnock, but individual females specialize in a single species. Genes regulating egg coloration appear to be passed down exclusively along the maternal line, allowing females to lay mimetic eggs in the nest of the species they specialize in. Females generally parasitize nests of the species which raised them. Male common cuckoos fertilize females of all lines, which maintains sufficient gene flow among the different maternal lines to prevent speciation.[10]

The mechanisms of host selection by female cuckoos are somewhat unclear, though several hypotheses have been suggested in attempt to explain the choice. These include genetic inheritance of host preference, host imprinting on young birds, returning to place of birth and subsequently choosing a host randomly ("natal philopatry"), choice based on preferred nest site (nest-site hypothesis), and choice based on preferred habitat (habitat-selection hypothesis). Of these hypotheses the nest-site selection and habitat selection have been most supported by experimental analysis.[10][11]

Adaptations for parasitism

Four clutches of reed warbler eggs, each containing one (larger) cuckoo egg

Among specialist avian brood parasites, mimetic eggs are a nearly universal adaptation. The generalist brown-headed cowbird may have evolved an egg coloration mimicking a number of their hosts.[12] Size may also be important for the incubation and survival of parasitic species; it may be beneficial for parasitic eggs to be similar in size to the eggs of the host species.[13]

The eggshells of brood parasites are often thicker than those of the hosts. For example, the eggs of cuckoos are about 23.2 micrometres (0.00091 in) thicker than those the great reed warbler.[14] The function of this thick eggshell is debated. One hypothesis, the puncture resistance hypothesis, states that the thicker eggshells serve to prevent hosts from breaking the eggshell, thus killing the embryo inside. This is supported by a study in which marsh warblers damaged their eggs more often when attempting to break cuckoo eggs, but incurred less damage when trying to puncture great reed warbler eggs put in the nest by researchers. Another hypothesis is the laying damage hypothesis, which postulates that the eggshells are adapted to damage the eggs of the host when the former is being laid, and prevent the parasite's eggs from being damaged when the host lays its eggs.[15] In support of this hypothesis, eggs of the shiny cowbird parasitizing the house wren and the chalk-browed mockingbird and the brown-headed cowbird parasitizing the house wren and the red-winged blackbird damaged the host's eggs when dropped, and sustained little damage when host eggs were dropped on them.[16]

Most avian brood parasites have very short egg incubation periods and rapid nestling growth. In many brood parasites, such as cuckoos and honeyguides, this short egg incubation period is due to internal incubation periods up to 24 hours longer in cuckoos than hosts. Some non-parasitic cuckoos also have longer internal incubation periods, suggesting that this longer internal incubation period was not an adaptation following brood parasitism, but predisposed birds to become brood parasites.[17] This is likely facilitated by a heavier yolk in the egg providing more nutrients. Being larger than the hosts at growth is a further adaptation to being a brood parasite.[14]

Mafia hypothesis

There is a question as to why the majority of the hosts of brood parasites care for the nestlings of their parasites. Not only do these brood parasites usually differ significantly in size and appearance, but it is also highly probable that they reduce the reproductive success of their hosts. The "mafia hypothesis" evolved through studies in an attempt to answer this question. This hypothesis revolves around host manipulations induced by behaviors of the brood parasite. Upon the detection and rejection of a brood parasite's egg, the host's nest is destroyed and nestlings injured or killed. This threatening response indirectly enhances selective pressures favoring aggressive parasite behavior that may result in positive feedback between mafia-like parasites and compliant host behaviors.[18]

There are two avian species that have been speculated to portray this mafia-like behavior: the brown-headed cowbird of North America, Molothrus ater, and the great spotted cuckoo of Europe, Clamator glandarius. The great spotted cuckoo lays the majority of its eggs in the nests of the European magpie, Pica pica. It repeatedly visits the nests that it has parasitised, a precondition for the mafia hypothesis.[18] An experiment was run by Soler et al. from April to July 1990 – 1992 in the high-altitude plateau Hoya de Guadix, Spain. They observed the effects of the removal of cuckoo eggs on the reproductive success of the magpie and measured the magpie's reaction; the egg was considered accepted if it remained in the nest, ejected if gone in between visits, or abandoned if eggs were present but cold. If any nest contents were gone between consecutive visits, the nests were considered to have been depredated. The magpie's reproductive success was measured by number of nestlings that survived to their last visit, which was just before the nestling had been predicted to fledge from the nest. The results from these experiments show that after the removal of the parasitic eggs from the great spotted cuckoo, these nests are predated at much higher rates than those where the eggs were not removed. Through the use of plasticine eggs that model those of the magpie, it was confirmed that the nest destruction was caused by the great spotted cuckoo. This destruction benefits the cuckoo, for the possibility of re-nesting by the magpie allows another chance for the cuckoo egg to be accepted.[18]

A similar experiment was done in 1996–2002 by Hoover et al. on the relationship between the parasitic brown-headed cowbird and a host, the prothonotary warbler, Protonotaria citrea. In their experiment, researchers manipulated the cowbird egg removal and cowbird access to the warbler's predator–proof nests.[19] They found that 56% of egg-ejected nests were predated upon, in comparison to 6% of non-ejected nests when cowbirds were not prevented from getting to the hosts' nest; nearly all nests protected from cowbirds fledged warblers successfully.[19] Of the nests that were rebuilt by hosts that had previously been predated upon, 85% of those were destroyed.[19] The number of young produced by the hosts that ejected eggs dropped 60% compared to those that accepted the cowbird eggs.

Nest-site hypothesis

In this hypothesis, female cuckoos select a group of host species with similar nest sites and egg characteristics to her own. This population of potential hosts is monitored and a nest is chosen from within this group.[20]

Research of nest collections has illustrated a significant level of similarity between cuckoo eggs and typical eggs of the host species. A low percentage of parasitized nests were shown to contain cuckoo eggs not corresponding to the specific host egg morph. In these mismatched nests a high percent of the cuckoo eggs were shown to correlate to the egg morph of another host species with similar nesting sites. This has been pointed to as evidence for nest- site selection.[20]

A criticism of the hypothesis is that it provides no mechanism by which nests are chosen, or which cues might be used to recognize such a site.[21]

Parental-care parasitism

Parental-care parasitism emphasizes the relationship between the host and the parasite in brood parasitism. Parental-care parasitism occurs when individuals raise offspring of other unrelated individuals. The host are the parents of offspring and the parasites are individuals who take advantage of either the nest or eggs within the family construct. Such dynamics occur when the parasites attempt to reduce their parental investment so they can invest the extra energy into other endeavors.[22]

Cost to the hosts

Given the harm that avian brood parasites can do to their hosts' reproductive success, hosts have come up with various defenses against this unique threat. Given that the cost of egg removal concurrent with parasitism is unrecoverable, the best strategy for hosts is to avoid parasitism in the first place. This can take several forms, including selecting nest sites which are difficult to parasitize, starting incubation early so they are sitting on the nests when parasites visit them early in the morning, and aggressively defending their territory.[citation needed] Despite providing intensive parental care, in Prothonotary Warblers, where conspecific brood parasitism occurs, there was no cost for host females in terms of annual survival probability.[23]

Hosts reject offspring

The host may be the one that ultimately ends up raising offspring after they return from foraging. Once parasitism has occurred, the next most optimal defense is to eject the parasitic egg. According to parental investment theory, the host can possibly adopt some defense to protect their own eggs if they distinguish which eggs are not theirs. Recognition of parasitic eggs is based on identifying pattern differences or changes in the number of eggs.[24] This can be done by grasp ejection if the host has a large enough beak, or otherwise by puncture ejection. Ejection behaviour has some costs however, especially when host species have to deal with mimetic eggs. Hosts may mistake one of their own eggs for a parasite's on occasion and eject it, and may damage their own eggs while trying to eject a parasite's egg.[25]

Among hosts not exhibiting parasitic egg ejection, some abandon parasitized nests and start over again. However, at high enough parasitism frequencies, this becomes maladaptive as the new nest will most likely also be parasitized. Some host species modify their nests to exclude the parasitic egg, either by weaving over the egg or in some cases rebuilding a new nest over the existing one. For instance, American coots may kick the parasites' eggs out, or build a new nest beside the brood nests where the parasites’ babies starve to death.[26] In the Western Bonelli's warbler Phylloscopus bonelli, a small host, experimental parasitism revealed that small dummy parasitic eggs were always ejected, whilst with large dummy parasitic eggs nest desertion more frequently occurred.[27]

Cost to the parasites

While parental-care parasitism significantly increased the breeding number of the parasite, only about half of the parasite eggs survived.[26] Parasitism for the individual (the brood parasite) also has significant drawbacks. As an example, the parasitic offspring of the bearded tits, Panurus biarmicus, compared to the offspring in non-parasitic nests, tend to develop much more slowly and often don't reach full maturity.[28] Parasitic females however can adopt either floater traits or nesting traits. Floater females are entirely dependent on others to raise their eggs because they do not have their own nests. Hence, they reproduce significantly less because the hosts reject their ‘intruder’ eggs or they may just miss the egg-laying period of the bird they are trying to pass their eggs to. Nesting females who have their own nests may also be parasitic due to temporary situations like sudden loss of nests, or they lay surplus eggs, which overload their parental care ability.[citation needed]

Hosts raise offspring

Sometimes hosts are completely unaware that they are caring for a bird that is not their own. This most commonly occurs because the host cannot differentiate the parasitic eggs from their own. It may also occur when hosts temporarily leave the nest after laying the eggs. The parasites lay their own eggs into these nests so their nestlings share the food provided by the host. It may occur in other situations. For example, female eiders would prefer to lay eggs in the nests with one or two existing eggs of others because the first egg is the most vulnerable to predators.[29] The presence of others’ eggs reduces the probability that a predator will attack her egg when a female eider leaves the nest after laying the first egg.

Sometimes, the parasitic offspring kills the host nest-mates during competition for resources. As an example, the parasite offspring of the cowbird chick kill the host nest-mates if food intake for each of them is low, but do not do so if the food intake is adequate, as a result of their interactions with co-inhabitants of the nest.[30]

Fish

Mouthbrooding parasites

Synodontis multipunctatus

A mochokid catfish of Lake Tanganyika, Synodontis multipunctatus, is a brood parasite of several mouthbrooding cichlid fish. The catfish eggs are incubated in the host's mouth, and—in the manner of cuckoos—hatch before the host's own eggs. The young catfish eat the host fry inside the host's mouth, effectively taking up virtually the whole of the host's parental investment.[31][32]

"Nest" parasites

A cyprinid minnow, Pungtungia herzi is a brood parasite of the percichthyid freshwater perch Siniperca kawamebari, which live in the south of the Japanese islands of Honshu, Kyushu and Shikoku, and in South Korea. Host males guard territories against intruders during the breeding season, creating a patch of reeds as a spawning site or "nest". Females (one or more per site) visit the site to lay eggs, which the male then defends. The parasite's eggs are smaller and stickier than the host's. 65.5% of host sites were parasitised in a study area.[33]

Insects

Kleptoparasites

A cuckoo bee from the genus Nomada
Main article: Kleptoparasitism

There are many different types of cuckoo bees, all of which lay their eggs in the nest cells of other bees, but they are normally referred to as kleptoparasites (Greek: klepto-, to steal), rather than as brood parasites, because the immature stages are almost never fed directly by the adult hosts. Instead, they simply take food gathered by their hosts. Examples of cuckoo bees are Coelioxys rufitarsis, Melecta separata, Nomada and Epeoloides.[34]

Kleptoparasitism in insects is not restricted to bees; several lineages of wasp including most of the Chrysididae, the cuckoo wasps, are kleptoparasites. The cuckoo wasps lay their eggs in the nests of other wasps, such as those of the potters and mud daubers.[35]

True brood parasites

Further information: Nest usurpation and Myrmecophily

True brood parasitism is rare among insects. Cuckoo bumblebees (the subgenus Psithyrus) are among the few insects which, like cuckoos and cowbirds, are fed by adult hosts. Their queens kill and replace the existing queen of a colony of the host species then use the host workers to feed their brood.[36]

Nest of Polistes dominula, host to the cuckoo wasp Polistes sulcifer

A true brood-parasitic wasp is Polistes sulcifer. This paper wasp has lost the ability to build its own nest, and relies on its host, Polistes dominula, to raise its brood. The adult host feeds the parasite larvae directly, unlike typical kleptoparasitic insects.[37][38]

In the bee Euglossa cordata, dominant reproductive females are brood parasitic, since they replace their daughter's eggs with their own eggs, diverting her resources from producing grand-offspring to producing more of their own offspring. In addition, to increase her longevity and fecundity, a mother also eats her daughter's eggs.[39]

Host insects are sometimes tricked into bringing offspring of another species into their own nests, as with the parasitic butterfly, Phengaris rebeli, and the host ant Myrmica schencki.[40] The butterfly larvae release chemicals that confuse the host ant into believing that the P. rebeli larvae are actually ant larvae.[40] Thus, the M. schencki ants bring back the P. rebeli larvae to their nests and feed them, much like the chicks of cuckoos and other brood-parasitic birds. This is also the case for the parasitic butterfly, Niphanda fusca, and its host ant Camponotus japonicus. The butterfly releases cuticular hydrocarbons (CHCs) that mimic the CHCs of the host male ant. The ant then brings the third instar larva back into its own nest and raises them until pupation.[41]

See also

References

  1. ^ Attenborough, David (1998). The Life of Birds. Princeton University Press. p. 246. ISBN 978-0-691-01633-7.
  2. ^ Payne, Robert B. (1997). "Avian brood parasitism". In Clayton, Dale H.; Moore, Janice (eds.). Host-parasite evolution: General principles and avian models. Oxford University Press. pp. 338–369. ISBN 978-0-19-854892-8.
  3. ^ Rothstein, Stephen I. (1990). "A Model System for Coevolution: Avian Brood Parasitism". Annual Review of Ecology and Systematics. 21: 481–508. doi:10.1146/annurev.ecolsys.21.1.481. JSTOR 2097034.
  4. ^ Stevens, Martin (2013-10-21). "Bird brood parasitism". Current Biology. 23 (20): R909–R913. doi:10.1016/j.cub.2013.08.025. ISSN 0960-9822. PMID 24156805.
  5. ^ Yezerinac, Stephen M.; Weatherhead, Patrick J. (1997). "Extra-Pair Mating, Male Plumage Coloration and Sexual Selection in yellow warblers (Dendroica petechia)". Proc. R. Soc. Lond. B. 264 (1381): 527–532. doi:10.1098/rspb.1997.0075. PMC 1688387.
  6. ^ Andersson, Malte; Eriksson, Mats O. G. (1982). "Nest Parasitism in Goldeneyes Bucephala clangula: Some Evolutionary Aspects". The American Naturalist. 120 (1): 1–16. doi:10.1086/283965. JSTOR 2461081.
  7. ^ Aragon; Moller; Soler; Soler (1999). "Molecular phylogeny of cuckoos supports a polyphyletic origin of brood parasitism". Journal of Evolutionary Biology. 12 (3): 495–506. doi:10.1046/j.1420-9101.1999.00052.x. S2CID 16923328.
  8. ^ Sorenson, Michael D.; Payne, Robert B. (2001). "A Single Ancient Origin of Brood Parasitism in African Finches: Implications for Host-Parasite Coevolution" (PDF). Evolution. 55 (12): 2550–67. doi:10.1554/0014-3820(2001)055[2550:asaoob]2.0.co;2. hdl:2027.42/72018. PMID 11831669.
  9. ^ Sorenson, Michael D.; Payne, Robert B. (2002). "Molecular Genetic Perspectives on Avian Brood Parasitism". Integrative and Comparative Biology. 42 (2): 388–400. doi:10.1093/icb/42.2.388. PMID 21708732.
  10. ^ a b Vogl, Wolfgang; Taborsky, Michael; Taborsky, Barbara; Teuschl, Yvonne; Honza, Marcel (2002). "Cuckoo females preferentially use specific habitats when searching for host nests". Animal Behaviour. 64 (6): 843–50. doi:10.1006/anbe.2003.1967. S2CID 17818119.
  11. ^ Teuschl, Yvonne; Taborsky, Barbara; Taborsky, Michael (1998). "How do cuckoos find their hosts? The role of habitat imprinting". Animal Behaviour. 56 (6): 1425–1433. doi:10.1006/anbe.1998.0931. PMID 9933539. S2CID 25931055.
  12. ^ Peer, Brian; Robinson, Scott; Herkert, James (2000). "Egg Rejection by Cowbird Hosts in Grasslands". The Auk. 117 (4): 892–901. doi:10.1642/0004-8038(2000)117[0892:ERBCHI]2.0.CO;2.
  13. ^ Krüger, Oliver (2007). "Cuckoos, cowbirds and hosts: Adaptations, trade-offs and constraints". Philosophical Transactions of the Royal Society B: Biological Sciences. 362 (1486): 1873–86. doi:10.1098/rstb.2006.1849. PMC 2442387. PMID 17827098.
  14. ^ a b Hargitai, Rita; Moskát, Csaba; Bán, Miklós; Gil, Diego; López-Rull, Isabel; Solymos, Emese (2010). "Eggshell characteristics and yolk composition in the common cuckoo Cuculus canorus: are they adapted to brood parasitism?". Journal of Avian Biology. 41 (2): 177–185. doi:10.1111/j.1600-048X.2009.04818.x. ISSN 0908-8857. S2CID 55241987.
  15. ^ Antonov, Anton; Stokke, Bård G.; Moksnes, Arne; Kleven, Oddmund; Honza, Marcel; Røskaft, Eivin (2006). "Eggshell strength of an obligate brood parasite: a test of the puncture resistance hypothesis". Behavioral Ecology and Sociobiology. 60 (1): 11–18. doi:10.1007/s00265-005-0132-6. ISSN 0340-5443.
  16. ^ López, Analía V; Fiorini, Vanina D; Ellison, Kevin; Peer, Brian D (2018). "Thick eggshells of brood parasitic cowbirds protect their eggs and damage host eggs during laying". Behavioral Ecology. 29 (4): 965–973. doi:10.1093/beheco/ary045. ISSN 1045-2249.
  17. ^ Birkhead, T. R.; Hemmings, N.; Spottiswoode, C. N.; Mikulica, O.; Moskat, C.; Ban, M.; Schulze-Hagen, K. (2010). "Internal incubation and early hatching in brood parasitic birds". Proceedings of the Royal Society B: Biological Sciences. 278 (1708): 1019–24. doi:10.1098/rspb.2010.1504. JSTOR 41148724. PMC 3049026. PMID 20880882.
  18. ^ a b c Soler, M.; Soler, J. J.; Martinez, J. G.; Moller, A. P. (1995). "Magpie Host Manipulation by Great Spotted Cuckoos: Evidence for an Avian Mafia?". Evolution. 49 (4): 770–775. doi:10.2307/2410329. JSTOR 2410329. PMID 28565143.
  19. ^ a b c Hoover, Jeffrey P.; Robinson, Scott K. (2007). "Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs". Proceedings of the National Academy of Sciences. 104 (11): 4479–83. doi:10.1073/pnas.0609710104. JSTOR 25426858. PMC 1838626. PMID 17360549.
  20. ^ a b Moksnes, Arne; Øskaft, Eivin R. (1995). "Egg-morphs and host preference in the common cuckoo (Cuculus canorus): An analysis of cuckoo and host eggs from European museum collections". Journal of Zoology. 236 (4): 625–48. doi:10.1111/j.1469-7998.1995.tb02736.x.
  21. ^ Vogl, Wolfgang; Taborsky, Michael; Taborsky, Barbara; Teuschl, Yvonne; Honza, Marcel (2002). "Cuckoo females preferentially use specific habitats when searching for host nests". Animal Behaviour. 64 (6): 843–50. doi:10.1006/anbe.2003.1967. S2CID 17818119.
  22. ^ Roldán, María; Soler, Manuel (2011). "Parental-care parasitism: How do unrelated offspring attain acceptance by foster parents?". Behavioral Ecology. 22 (4): 679–91. doi:10.1093/beheco/arr041.
  23. ^ Tucker, A.M.; Bulluck, L.P. (2018). "No evidence for a negative effect of conspecific brood parasitism on annual survival of female Prothonotary Warblers". Ibis. 160 (2): 447–452. doi:10.1111/ibi.12538.
  24. ^ Lyon, Bruce E. (2003). "Egg recognition and counting reduce costs of avian conspecific brood parasitism". Nature. 422 (6931): 495–9. doi:10.1038/nature01505. PMID 12673243.
  25. ^ Lorenzana, Janice C.; Sealy, Spencer G. (2001). "Fitness costs and benefits of cowbird egg ejection by gray catbirds". Behavioral Ecology. 12 (3): 325–9. doi:10.1093/beheco/12.3.325.
  26. ^ a b Lyon, Bruce E (1993). "Conspecific brood parasitism as a flexible female reproductive tactic in American coots". Animal Behaviour. 46 (5): 911–28. doi:10.1006/anbe.1993.1273. S2CID 53188986.
  27. ^ Roncalli, Gianluca; Ibáñez-Álamo, Juan Diego; Soler, Manuel (2017). "Size and material of model parasitic eggs affect the rejection response of Western Bonelli's Warbler Phylloscopus bonelli". Ibis. 159 (1): 113–23. doi:10.1111/ibi.12431.
  28. ^ Hoi, Herbert; Krištofík, Jan; Darolová, Alzbeta (2010). "Conspecific brood parasitism and anti-parasite strategies in relation to breeding density in female bearded tits". Behaviour. 147 (12): 1533–49. doi:10.1163/000579510X511060. JSTOR 20799565.
  29. ^ Robertson, Gregory J. (1998). "Egg adoption can explain joint egg-laying in common eiders". Behavioral Ecology and Sociobiology. 43 (4–5): 289–96. doi:10.1007/s002650050493. JSTOR 4601519.
  30. ^ Gloag, Ros; Tuero, Diego T.; Fiorini, Vanina D.; Reboreda, Juan C.; Kacelnik, Alex (2012). "The economics of nestmate killing in avian brood parasites: A provisions trade-off". Behavioral Ecology. 23 (1): 132–40. doi:10.1093/beheco/arr166. S2CID 3945653.
  31. ^ Sato, Tetsu (1986). "A brood parasitic catfish of mouthbrooding cichlid fishes in Lake Tanganyika". Nature. 323 (6083): 58–9. doi:10.1038/323058a0. PMID 3748180.
  32. ^ Blažek, Radim; Polačik, Matej; Smith, Carl; Honza, Marcel; Meyer, Axel; Reichard, Martin (2018). "Success of cuckoo catfish brood parasitism reflects coevolutionary history and individual experience of their cichlid hosts". Science Advances. 4 (5): eaar4380. doi:10.1126/sciadv.aar4380. PMC 5931752. PMID 29732407. {{cite journal}}: Unknown parameter |lay-url= ignored (help); Unknown parameter |laydate= ignored (help); Unknown parameter |laysource= ignored (help)
  33. ^ Baba, Reiko; Nagata, Yoshikazu; Yamagishi, Satoshi (1990). "Brood parasitism and egg robbing among three freshwater fish". Animal Behaviour. 40 (4): 776–8. doi:10.1016/s0003-3472(05)80707-9.
  34. ^ Pawelek, Jaime; Coville, Rollin. "Cuckoo Bees". UC Berkeley. Retrieved 24 February 2015.
  35. ^ "Cuckoo Wasps". Western Australian Museum. Retrieved 24 February 2015.
  36. ^ Kawakita, Atsushi; Sota, Teiji; Ito, Masao; Ascher, John S.; Tanaka, Hiroyuki; Kato, Makoto; Roubik, David W. (2004). "Phylogeny, historical biogeography, and character evolution in bumble bees (Bombus: Apidae) based on simultaneous analysis of three nuclear gene sequences". Molecular Phylogenetics and Evolution. 31 (2): 799–804. doi:10.1016/j.ympev.2003.12.003. PMID 15062814.
  37. ^ Dapporto, L; Cervo, R; Sledge, M. F.; Turillazzi, S. (2004). "Rank integration in dominance hierarchies of host colonies by the paper wasp social parasite Polistes sulcifer (Hymenoptera, Vespidae)". Journal of Insect Physiology. 50 (2–3): 217–23. doi:10.1016/j.jinsphys.2003.11.012. PMID 15019524.
  38. ^ Ortolani, Irene; Cervo, Rita (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.
  39. ^ Cameron, Sydney A. (2004). "Phylogeny and Biology of Neotropical Orchid Bees (Euglossini)". Annual Review of Entomology. 49: 377–404. doi:10.1146/annurev.ento.49.072103.115855. PMID 14651469.
  40. ^ a b Akino, T.; Knapp, J. J.; Thomas, J. A.; Elmes, G. W. (1999). "Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies". Proceedings of the Royal Society B: Biological Sciences. 266 (1427): 1419–26. doi:10.1098/rspb.1999.0796. JSTOR 51672. PMC 1690087.
  41. ^ Hojo, Masaru K.; Wada-Katsumata, Ayako; Akino, Toshiharu; Yamaguchi, Susumu; Ozaki, Mamiko; Yamaoka, Ryohei (2009). "Chemical disguise as particular caste of host ants in the ant inquiline parasite Niphanda fusca (Lepidoptera: Lycaenidae)". Proceedings of the Royal Society B: Biological Sciences. 276 (1656): 551–8. doi:10.1098/rspb.2008.1064. PMC 2664337. PMID 18842547.
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