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==== [[Caecilia]]ns ====
==== [[Caecilia]]ns ====
Caecilians are the only vertebrate animals with well-documented matriphagous behaviours. In viviparous caecilians the young consume the mother's [[oviduct]] lining by scraping it off with their teeth. In at least one species, ''[[Boulengerula taitana]]'', the young feed on the mother's skin by tearing it off with their teeth, which then regenerates within a few days.<ref>Kupfer, Alex; Muller, Hendrik; Antoniazzi, Marta M.; Jared, Carlos; Greven, Hartmut; Nussbaum, Ronald A.; Wilkinson, Mark (2006). "Parental investment by skin feeding in a caecilian amphibian". Nature. 440 (7086): 926–929. doi:10.1038/nature04403. PMID 16612382.</ref>
Caecilians are the only vertebrate animals with well-documented matriphagous behaviours. In viviparous caecilians the young consume the mother's [[oviduct]] lining by scraping it off with their teeth. In at least two species, ''[[Boulengerula taitana]]'' and ''[[Siphonops annulatus]]'', the young feed on the mother's skin by tearing it off with their teeth, which then regenerates within a few days.<ref>Kupfer, Alex; Muller, Hendrik; Antoniazzi, Marta M.; Jared, Carlos; Greven, Hartmut; Nussbaum, Ronald A.; Wilkinson, Mark (2006). "Parental investment by skin feeding in a caecilian amphibian". Nature. 440 (7086): 926–929. doi:10.1038/nature04403. PMID 16612382.</ref> Because neither are closely related, either this behaviour is more common than currently observed or it evolved independently.<ref>Mark Wilkinson; et al. (June 2008). "One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona)". Biology Letters. 4 (4): 358–61. doi:10.1098/rsbl.2008.0217. PMC 2610157. PMID 18547909.</ref>


== Evolution ==
== Evolution ==

Revision as of 22:43, 7 November 2018

Matriphagy is the consumption of the mother by her offspring.[1][2] The behavior generally takes place within the first few weeks of life and has been documented in some species of insects, nematode worms, scorpions, and other arachnids as well as in caecilian amphibians.[3][4][5]

Stegodyphus lineatus, one of the best described species that participates in matriphagy.

The specifics of how matriphagy occurs varies among different species, but the process is best described in Stegodyphus lineatus, where the mother harbors nutritional resources for her young through food consumption. The mother is able to regurgitate small portions for her growing offspring, but between 1-2 weeks after hatching the progeny capitalize on this food source by eating her alive. Typically, offspring only feed on their biological mother as opposed to other females in the population.

Spiders that engage in matriphagy produce offspring with higher weights, shorter and earlier moulting time, larger body mass at dispersal, and higher survival rates than clutches deprived of matriphagy. In some species, matriphagous offspring were also more successful at capturing large prey items and had a higher survival rate at dispersal. These benefits to offspring outweigh the cost of survival to the mothers and help ensure that her genetic material is passed to the next generation, thus perpetuating the behavior.[6][7][8][9]

Overall, matriphagy is an extreme form of parental care that stands in stark contrast to other forms such as extended parental care and protection found in arachnids and other insects. The uniqueness of this phenomenon has led to several expanded analogies in human culture and contributed to the pervasive fear of spiders throughout society.

Etymology

Matriphagy can be broken down into two components:

  • Matri (mother)
  • Phagy (to feed on)

Description of behavior

Matriphagy behavior generally consists of offspring consuming their mother; however, different species exhibit different variations of this behavior.

Spiders

Amaurobius ferox

Black lace-weaver (Amaurobius ferox)

In Amaurobius ferox, offspring do not immediately consume their mother. One day after the offspring emerge from their eggs, their mother lays another set of eggs, known as trophic eggs.[10] These eggs are very nutritious and, as a result, are consumed by the offspring. Another three days later, the mother becomes reserved and away from her offspring.[10] Then, around the fourth day, matriphagy behavior commences when the mother begins using web vibrations to communicate between to her offspring.[10][11] These web vibrations tell the offspring to move towards her abdomen. The mother will also begin to drum and jump on the web as communication.[10] Through these behaviors, offspring may be able to detect when and where to consume their mother. After completing their first molt and communicating with their mother, the offspring migrate towards her and a couple of the spiderlings jump onto her back with the goal of consuming her.[10] In response to her offspring, the mother attempts to keep her offspring off of her by utilizing her legs and starts jumping and drumming more.[10] Approximately 20-30 minutes before her consummation, the mother increases the frequency of her jumps and drumming, while the offspring tries even harder to get onto her back.[10] Then, the mother presses her body onto the offspring and relaxes her whole body and allows her offspring to consume her.[10] Her offspring all begin consummation from her abdomen and suck on her insides for one hour.[10] As they consumed her, they also released poison into her body through their bites, which caused a quick death.[10] The mother’s body is kept for a few weeks as a nutritional reserve.[10]

Interestingly, matriphagy behavior in this species is dependent on the developmental stage that the offspring are currently at.[10] If offspring that are older than four days old are given to an unrelated mother, they refuse to consume her.[10] However, if younger offspring are placed with an unrelated mother, they readily consume her.[10] If a mother loses her offspring, she is actually able to produce another clutch of offspring.[10]

Diaea ergandros

The mothers of Diaea ergandros can only lay one clutch, unlike Amaruobius ferox.[9] However, they invest a lot of time and energy into storing nutrients and food into large oocytes, known as trophic eggs, similar to Amaruobius ferox.[9] However, these trophic eggs stay within the mother, due to being so large that they cannot physically come out her body.[9] Some of the nutrients are converted into haemolymph, which can be consumed through the mother’s leg joints, since it has been liquefied.[9] Her offspring suck small amounts of the haemolymph from her leg joints continuously over time, causing the mother to gradually shrink until she becomes immobile and dies.[9][10] In this species, it has been shown that this matriphagy behavior may contribute to reducing cannibalism by siblings.[9]

Stegodyphus lineatus

Right after hatching, these hatchlings are unable to catch and ingest prey on their own. Because of this, they rely upon their mother to provide them with food and nutrients. Their mother does this by regurgitating her bodily fluids containing a mixture of nutrients for them to feed on. This process begins early during mating, which increases the mother’s production of digestive enzymes to better digest her prey. Consequently, this helps her retain more nutrients for her offspring to consume her later. The mother’s midgut tissues start to slowly degrade during the incubation period of her eggs. After her offspring hatch, she regurgitates food for them to feed from with the help of her already-liquefied midgut tissues and discontinues consumption of prey for herself. Meanwhile, her midgut tissues continue to degrade into a liquid state to maximize the amount of nutrients from the mother’s body. As degradation continues, nutritional vacuoles form within her abdomen to amass all of the nutrients. These nutritional vacuoles are the first portion of the mother that is consumed by her offspring. Her offspring puncture her abdomen and suck up the vacuoles. After approximately 2-3 hours, the mother’s bodily fluids are completely consumed, and only her exoskeleton is left.[11]

This species is only able to have one clutch, which might explain why so much time and energy is spent on taking care of offspring. Furthermore, matriphagy behavior can also occur between offspring and mothers who have recently laid eggs that are not related.[11]

Hump Earwig

Anechura harmandi

Mothers in this species have been found to reproduce early in the year when it is still cold.[12] This is mainly for the purpose of avoiding predation. This is important to them, because once females have laid one clutch, they cannot produce a second.[12] Because of the cold temperature, there is a scarcity of available nutrients when the offspring hatch. It has been predicted that the mother is the next best option for these offspring to gain enough nutrients to live, which is necessary for survival.[12]

Pseudoscorpions

A group of pseudoscorpions (Paratemnoides nidificator)

Paratemnoides nidificator

Matriphagy behavior in this species is usually observed during times of food scarcity.[13] After their offspring hatch, mothers exit their nests and await to be consumed by their offspring.[13] Offspring follow their mothers out of the nest and grab onto her legs. They then proceed to feed through her leg joints, similar to that of Diaea ergandros.[13] After consumption of their mother’s insides, they throw her exoskeleton out of the nest.[13]

Females of this species are able to produce more than one clutch of offspring.[13]

Additionally, matriphagy in this species has been predicted to prevent cannibalism as well.[13]

Vertebrates

Caecilians

Caecilians are the only vertebrate animals with well-documented matriphagous behaviours. In viviparous caecilians the young consume the mother's oviduct lining by scraping it off with their teeth. In at least two species, Boulengerula taitana and Siphonops annulatus, the young feed on the mother's skin by tearing it off with their teeth, which then regenerates within a few days.[14] Because neither are closely related, either this behaviour is more common than currently observed or it evolved independently.[15]

Evolution

The adaptive value of matriphagy is based on the benefits provided to the offspring and the costs borne by the mother. Functionally analyzing matriphagy in this manner will help shed light on why this unusual and extreme form of care has evolved and been selected for.

Benefits to offspring

  • Consuming the mother is a source of nutrition which is important for growth and development [10].
  • The body mass and opisthosoma length of spiderlings increases (2.5 fold) after matriphagy compared to before (opisthosoma is the posterior part of the body in spiders, analogous to the abdomen). Additionally, body mass tends to be higher for spiderlings that engage in matriphagy as compared to those that do not [8][10].
  • Matriphagy advances molting time. Molting is the growing of a larger exoskeleton and shedding the old one. Advancement of molting time means that the spiders are growing at a faster rate [10].
  • Matriphagous spiderlings tend to experience significantly greater survival rates and fitness compared to non-matriphagous offspring at dispersal [7][10][12].
  • Matriphagous spiderlings hunt larger prey and show much complete prey consumption than non-matriphagous spiderlings [10].
  • Matriphagy improves sociality in spiders, primarily by reducing sibling cannibalism [9].

Costs to the mother

Unlike other milder forms of parental care, matriphagy ends with the life of the mother, the gravest of all costs. So, why has it evolved? In order to answer this, it is important to look at costs to the mother in terms of reproductive output, egg sac development and number of young reared (i.e. are offspring more successful if the mother evades matriphagy and reproduces again?).

  • A study conducted in Amaurobius ferox showed that 79% of females separated prior to matriphagy produce second egg sacs and only 42% of these develop completely (compared to the >90% development of egg sacs in the first brood)[10].
  • Number of spiderlings in the second brood were significantly lower than in the first brood. Additionally, these individuals were also smaller than the spiders in the first brood [10].
  • Females that were offered the opportunity to successively lay two egg sacs had a lower expected output of dispersing offspring than females that were victims of matriphagy which produced only a single clutch [10].

Summary

In conclusion, spiderlings that engage in matriphagy benefit a lot more than spiderlings that do not engage in this behavior. Further, the progeny of females that escape matriphagy to lay a second brood are significantly less successful than those that ate their mother the first time around. Hence, it is more clear now as to why this unusual and extreme form of parenting has evolved and has been selected for.

Other forms of parental care

Unsurprisingly, matriphagy is not a universal process among arachnids. Arachnids, arthropods, and similar species that exhibit alternate methods of reproduction include Coelotes terrestris, Forficula auricularia, Euscorpius flavicaudis, and Xysticus bimaculatus.

Extended care in Coelotes terrestris

The ‘maternal social’ spider, Coelotes terrestris, utilizes extended maternal care as a reproductive model for its offspring. Upon laying the egg sac, a C. terrestris mother will stand guard and incubate the sac for 3 to 4 weeks. She will stay with her young from the time of their emergence until dispersal approximately 5 to 6 weeks after emergence from the egg sac. During the gregarious phase in which spider-lings develop, mothers will provide their offspring prey regulated by stimulation emerging from the ‘gregarious’ progeny.[16]

Protecting their egg sacs from predation and parasites yields a high benefit to cost ratio. It is reasonable to relate fitness of the mother to offspring developmental state—a higher condition of the mother will yield larger young that are better at surviving predation. The presence of the mother has a protective effect against parasitism. In addition, a mother can keep feeding while guarding progeny without any weight loss, collecting food for both herself and her offspring.[16]

Costs for protecting the egg sac are low, and upon separation from egg sacs, 90% of females have the energy sustenance to lay new sacs, although it does induce a time loss of several weeks.[16]

In experimental conditions, costs arose if maternal care was not provided, with egg sacs drying out and developing acaria and molds; thus, maternal care is essential for survival. Experimental food-deprived broods reared by the mother induced matriphagy, where 77% of offspring consumed their mother upon birth, suggesting that although matriphagy can exist, but the costs outweigh the benefits provided that mothers have sufficient access to resources. Matriphagy will only occur when a female is too old to rear another clutch.[16]

Mother-Offspring aggregation in the European earwig 

In Forficula auricularia, the European earwig, there exists an age-dependent coadaptation between parents and offspring. The behavior in this relationship is dynamic and timing of parental care affects how offspring will react, with the relationship providing a benefit to both the parent and the offspring. Since interaction is carried over extended periods of time, the behavioral patterns on offspring varies as offspring age changes—maternal care is beneficial, but not vital, for offspring survival.[17]

Care is most intense during the first larval instar as opposed to later points in development, and it is likely a result of the mother’s attempt at food provisioning. This has been measured through stability in aggregation levels between the parent and the offspring at early points in nymph development, with a sharp decline in aggregation levels as nymphs age and occasionally with when with different kin.[8]

In general, nymph survival and female-offspring aggregation do exhibit a positive correlation, especially when care is at its highest stages, which is often in the early stages of development.[17]

Parental care and production in Euscorpius flavicaudis

Maternal care in the scorpion Euscorpius flavicaudis is unique; offspring are viviparous and born relatively large after nourishment in utero. Mothers’ broods are large, weighing about 44% of her weight. Upon birth, offspring climb onto their mother’s dorsum until their first instar, or developmental phase, ends after about 7 days; during this time they cannot feed or defend themselves, and they can barely move. This reproductive habit is primarily involved for predation protection as opposed to food foraging.[18]

Presence of the mother has an effect on juvenile survival with regard to predation, since juveniles could be prey to conspecific scorpions. An absence of the mother would result in high brood mortality rates averaging 99%; thus, maternal protection is extremely important in this species. Females tend to have monogamous relationships with other conspecifics, only mating with one male.[18]

Extended care in the Australian crab spider 

Xysticus bimaculatus, the Australian crab spider, exhibits extended maternal care to enhance fitness of the mother’s offspring. The crab spiders are subsocial species, and produce extremely small clutches through the production of an egg sac. Small clutch size potentially reveals a limit in number of juveniles that a mother can successfully care for, indicating that mothers exhibit extensive maternal food provisioning.[19]

Regarding development, body size differs depending on the size of the nest group, indicating a relationship between available resources and favorable phenotype. Instar groups for early offspring are extremely important as well, since early instars benefit the most from maternal care. Offspring obtain crucial benefits beyond nutritional independence and still require extensive maternal food provisioning in these early stages.[19]

Studies indicate that mothers are a protective figure, as spider-ling attacks are considerably lower with the mother around. As mothers provide care and food provisioning; however, there is a noticeable change revealed through maternal weight loss of about 5 to 10%.[19]

The limit in clutch size suggests that X. bimaculatus is a good model for communal feeding in group-living spiders, which is the standard feeding model for 72.86% of observed feeding tactics among this species. Prey-sharing will occur regardless of maternal presence and reflects an exploitative feeding behavior.[19]

In extreme cases, maternal food provisioning can involve obligate or facultative matriphagy, depending on the severity of lack of resources.[19]

Cultural significance

Although matriphagy is not a widely circulated term in society, there are specific instances where it has been used to represent or symbolize specific ideas. For instance, Dr. Luke Winslow from San Diego State University dubbed the concept "rhetorical matriphagy' in 2017 in connection with critiques of increasing online higher education offerings. [20] In this analogy, higher education assumes the role of the mother, neoliberalism assumes the role of the hatchlings, and online education discourse assumes the role of the mother’s symbolic resources, which are used to attract hatchings and eventually lead them to engage in matriphagy for these resources. [20] Additionally, the theory behind the existence of matriphagy is strikingly similar to that of higher education. Matriphagy is a less than ideal survival mechanism in response to an environment with poor conditions and few natural resources, but it persists because of guaranteed survival of the mother’s genes via her hatchlings. [20] Similarly, online education does not consider itself at the same level as traditional forms of higher education but does provide an equal opportunity for all to attain such education in a cost-effective way that satisfies most stakeholders in the process. [20]

Those that have been exposed to matriphagy may be frightened by such a seemingly strange and bizarre natural behavior, especially since it is mainly observed in already feared organisms. Thus, matriphagy is often posed as perpetuation of a long held fear of arachnids in human society. [21]

In contrast, others may look to matriphagy as a leading example of purity, as it represents an instinctive form of altruism. Altruism in this case refers to an "intentional action ultimately for the welfare of others that entails at least the possibility of either no benefit or a loss to the actor," and is a highly popularized and desirable concept in many human cultures. [22] Matriphagy can be viewed as altruism, insofar as participating mothers "sacrifice" their survival for the welfare of their offspring. [22] Although participation in matriphagy is not truly an intentional action, mothers are nevertheless driven by natural selection pressures based on offspring fitness to engage in such behavior. [22] This in turn creates a cycle that perpetuates altruistic matriphagous behavior through generations. Such an example of altruism on a purely biological level differs severely from human standards of altruism, which are tainted by moral virtues such as rationality, trust, and reciprocity. [22]

List of species that engage in matriphagy

Spiders

Earwigs

  • Anechura harmandi

Pseudoscorpions

  • Paratemnoides nidificator

Vertebrates

References

  1. ^ a b "For Some Animals, Baby's First Meal is Its Mother". Mental Floss. Retrieved 2016-11-19.
  2. ^ "Zoologger: The baby spiders that munch up their mum". New Scientist. Retrieved 2017-03-23.
  3. ^ "Watch Baby Spiders Eat Their Mothers Alive". 2017-09-20. Retrieved 2018-03-22.
  4. ^ Engelhaupt, Erika (2014-02-06). "Some animals eat their moms, and other cannibalism facts". Science News. Retrieved 2018-03-22.
  5. ^ Kupfer, Alex; Muller, Hendrik; Antoniazzi, Marta M.; Jared, Carlos; Greven, Hartmut; Nussbaum, Ronald A.; Wilkinson, Mark (2006). "Parental investment by skin feeding in a caecilian amphibian". Nature. 440 (7086): 926–929. doi:10.1038/nature04403. PMID 16612382.
  6. ^ Toyama, Masatoshi (2003). "Relationship between reproductive resource allocation and resource capacity in the matriphagous spider, Chiracanthium japonicum (Araneae: Clubionidae)". Journal of Ethology. 21: 1–7. doi:10.1007/s10164-002-0067-6 – via Springer Link.
  7. ^ a b Salomon, Mor; Schneider, Jutta; Lubin, Yael (2005–2006). "Maternal investment in a spider with suicidal maternal care,Stegodyphus lineatus(Araneae, Eresidae)". Oikos. 109 (3): 614–622. doi:10.1111/j.0030-1299.2005.13004.x. ISSN 0030-1299.{{cite journal}}: CS1 maint: date format (link)
  8. ^ a b c Toyama, Masatoshi (March 1999). "Adaptive advantages of maternal care and matriphagy in a foliage spider,Chiracanthium japonicum (Araneae: Coubionidae)". Journal of Ethology. 17 (1): 33–39. doi:10.1007/bf02769295. ISSN 0289-0771.
  9. ^ a b c d e f g h Evans, Theodore A.; Wallis, Elycia J.; Elgar, Mark A. (July 1995). "Making a meal of mother". Nature. 376 (6538): 299–300, author reply 301. doi:10.1038/376299a0. ISSN 0028-0836. PMID 7630393.
  10. ^ a b c d e f g h i j k l m n o p q r s t u v w x Kim, Kil-Won; Horel, André (2010-04-26). "Matriphagy in the Spider Amaurobius ferox (Araneidae, Amaurobiidae): an Example of Mother-Offspring Interactions". Ethology. 104 (12): 1021–1037. doi:10.1111/j.1439-0310.1998.tb00050.x. ISSN 0179-1613.
  11. ^ a b c Salomon, M.; Aflalo, E. D.; Coll, M.; Lubin, Y. (2014). "Dramatic histological changes preceding suicidal maternal care in the subsocial spiderStegodyphus lineatus(Araneae: Eresidae)". Journal of Arachnology. 43 (1): 77–85. doi:10.1636/b14-15.1. ISSN 0161-8202.
  12. ^ a b c d Suzuki, Seizi; Kitamura, Masashi; Matsubayashi, Kei. "Matriphagy in the hump earwig, <Emphasis Type="Italic">Anechura harmandi</Emphasis> (Dermaptera: Forficulidae), increases the survival rates of the offspring" (PDF). Journal of Ethology. 23 (2). doi:10.1007/s10164-005-0145-7.pdf. ISSN 0289-0771.
  13. ^ a b c d e f Tizo-Pedroso, Everton; Del-Claro, Kleber (2005). "MATRIPHAGY IN THE NEOTROPICAL PSEUDOSCORPION PARATEMNOIDES NIDIFICATOR (BALZAN 1888) (ATEMNIDAE)". Journal of Arachnology. 33 (3): 873–877. doi:10.1636/s03-61.1. ISSN 0161-8202.
  14. ^ Kupfer, Alex; Muller, Hendrik; Antoniazzi, Marta M.; Jared, Carlos; Greven, Hartmut; Nussbaum, Ronald A.; Wilkinson, Mark (2006). "Parental investment by skin feeding in a caecilian amphibian". Nature. 440 (7086): 926–929. doi:10.1038/nature04403. PMID 16612382.
  15. ^ Mark Wilkinson; et al. (June 2008). "One hundred million years of skin feeding? Extended parental care in a Neotropical caecilian (Amphibia: Gymnophiona)". Biology Letters. 4 (4): 358–61. doi:10.1098/rsbl.2008.0217. PMC 2610157. PMID 18547909.
  16. ^ a b c d Gundermann, Jean-Luc; Horel, André; Roland, Chantal (2010-04-26). "Costs and Benefits of Maternal Care in a Subsocial Spider, Coelotes terrestris". Ethology. 103 (11): 915–925. doi:10.1111/j.1439-0310.1997.tb00133.x. ISSN 0179-1613.
  17. ^ a b Gómez, Y.; Kölliker, M. (Oct 2013). "Maternal care, mother-offspring aggregation and age-dependent coadaptation in the European earwig". Journal of Evolutionary Biology. 26 (9): 1903–1911. doi:10.1111/jeb.12184. ISSN 1420-9101. PMID 23937357.
  18. ^ a b Benton, T. G. (1991-01-01). "Reproduction and Parental Care in the Scorpion, Euscorpius Flavicaudis". Behaviour. 117 (1): 20–28. doi:10.1163/156853991X00102. ISSN 1568-539X.
  19. ^ a b c d e Dumke, Marlis (2016). "Extended maternal care and offspring interactions in the subsocial Australian crab spider, Xysticus bimaculatus". Australian Journal of Zoology. 64 (5): 344. doi:10.1071/zo16070. ISSN 0004-959X.
  20. ^ a b c d Winslow, Luke (28 Apr 2017). "Rhetorical Matriphagy and the Online Commodification of Higher Education". Western Journal of Communication. 81 (5): 582–600. doi:10.1080/10570314.2017.1316418.
  21. ^ Barness, Sarah (2 Jan 2014). "Spider Babies Eat Their Mother From The Inside Out, Giving Us Another Reason To Be Terrified Of Arachnids". HuffPost.
  22. ^ a b c d Montayne, James A. (2016). "Review of 'Does Altruism Exist? Culture, Genes, and the Welfare of Others'". The Independent Review. 20 (3).
  23. ^ Kim, Kil Won; Roland, Chantal; Horel, André (25 December 2001). "Functional Value of Matriphagy in the Spider Amaurobius ferox". Ethology. 106 (8): 729–742. doi:10.1046/j.1439-0310.2000.00585.x.
  24. ^ Koyanagi, Chie; Abé, Hiroshi (2016-08-07). "Offspring discrimination by female parents of the matriphagous spiderCheiracanthium japonicum(Araneae: Eutichuridae)". Journal of Natural History. 50 (41–42): 2573–2583. doi:10.1080/00222933.2016.1210689. ISSN 0022-2933.
  25. ^ Nuwer, Rachel (2015). "Mother, May I … Eat You?". Scientific American. 313 (4): 19. doi:10.1038/scientificamerican1015-19.
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