Parental care in birds

Archaeopteryx fossil in the Museum fur Naturkunde, Berlin, Germany^[1]

Parental care refers to the level of investment provided by the mother and the father to insure development and survival of their offspring. In most birds, parents invest profoundly in their offspring as a mutual effort, making a majority of them socially monogamous for the duration of the breeding season. This happens regardless of whether there is a paternal uncertainty.

Origin

Birds originally branched from theropod dinosaurs and underwent body miniaturization over a 50 million year period. Changes in anatomy are rearrangement of body mass, adults retain juvenile traits including large brain mass and eyes despite a smaller snout (paedomorphism), and aerial abilities. (Michael S. Y. Lee, Andrea Cau, Darren Naish, and Gareth J. Dyke)^[2]

The Archaeopteryx was the first bird with evolved feathers.^[3] The forelimb in the Archaeopteryx could have been used for parental care of offspring because enlarged feathers were possibly used to shield offspring from the suns' rays and for flight. (Carey, J.R., and Adams. J (2001))^[4]

Kavanau (1987) was the first to find that unique bi-parental care seen in modern birds probably evolved from extinct birds. They developed the ability to provide protection, escorting, nurturing and egg guarding abilities for their young. Evolution of homeothermy and flight most likely occurred in bi-parental birds with precocial chicks. Kavanau said extant birds (David J. Varricchio)^[5] evolved and learned flight through evolution to access ground nests faster. (Kavanau)^[6]

Van Rhijn (1984, 1990), Handford and Mares (1985), and Elzanowski (1985) were the first to announce the earliest form of parental care as being mono-parental male care.^{[7][8] [9]}

Wesolowsi (1994) contradicted Kavanau's reasoning by saying flight evolved due to parental care not reproduction as previously thought. While flight was being enhanced in evolutionary stages, lack of parental care meant that the increasing amount of large eggs required a higher level of investment. This created young that were able to take flight shortly after hatching which is known as precocial, in the form of unassisted paternal (male only) care. The next stage of evolution replaced this with bi-parental care (with a few exceptions). Ligon (1999) suggested with Vehrencamp (2000) that male incubation existed first and later gave way to shared and finally female only incubation.

A possible evolutionary timeline (Kavanau):

Theropod dinosaurs → Birds evolved unique bi-parental care→ Avian birds evolved homeothermy and flight

Burley and Johnson (2002), Tullberg et al. (2002), Prum (2002), and Varricchio et al. (1999) questioned the male evolutionary shift from no care to male care. They proposed like Kavanau's model that parental care came first leading to bi-parental care in extant birds.

The origin of parental care in birds is still a controversial topic today. (Tomasz Wesolowski )^[10]

Different modes of parental care

Bi-parental care

Bi-parental care is the most common form in birds, especially in passerines. A mating pair equally contributes to feeding and guarding the offspring. It occurs in approximately 85% of bird species.^[11] The hatchling benefits from the mutual care at the cost of the parents' future reproductive success. Each parent tries to find a mate who will not desert the nest and has high qualities that showcase their parental skills (e.g. ornamental cues). The good parent hypothesis states that birds can invest more energy towards their own survival rate by choosing an ideal mate.

Evolution in potential mates to advertise their parental strengths through ornamental cues (e.g. a yellow chest patch in Iberian rock sparrows) are based on the differential allocation hypothesis. This hypothesis states that the bigger the ornamental cue a mate has, the more investment is put towards the offspring. As a result of bi-parental care, the offspring are usually stronger than birds who are only cared for by one parent in Iberian rock sparrows. (Vicente García-Navas)^[12]

Maternal vs paternal care

In bi-parental care, the male provides food and the female is a caretaker. Both ensure the survival of the offspring. The female may care for her young by covering them to keep them warm, shielding them from the sun or from rain and guarding them from predation. The male may also feed the female, who in turn regurgitates the food to the chicks. In female red-eyed vireos the roles are reversed. Nonbreeding adults or juveniles in acorn woodpeckers contribute the care through collaboration with the parents. (Paul R. Ehrlich, David S. Dobkin, and Darryl Wheye)^[13]

Mono-parental care

Male only care occurs in only 1% of bird species (approximately 90 species). Female only care occurs in 8% of species (approximately 772 species). (Andrew Cockburn)^[14] A hypothesis states that the parent that invests less reproductive effort in comparison to its mate, will have a higher chance of deserting because it loses less if successful offspring are not produced. However, in some birds (such as the snail kite found in South America, the Caribbean and Florida), the male and the female sometimes compete over which one will desert the nest regardless of who has invested more into the reproductive effort. Robert Trivers (1972)^[15]

Parental care in polyandrous species

Polyandry care occurs in roughly 9% of bird species (approximately 852 species). (Andrew Cockburn)^[16] The two forms of polyandry are sequential and simultaneous polyandry. Sequential polyandry refers to the mating strategy females use in certain situations. First, they will mate with one male and raise the offspring for a short period of time. Then they will mate with another male and care for that clutch resulting in more genetic diversity and quantity of the offspring per season. Females never incubate offspring alone unless the male has been killed. Some examples of birds who practice sequential polyandry include spotted sandpipers and red-necked phalaropes. Temminck's stint, little stint, mountain plover, and sanderling are very similar because the females lay a clutch of eggs and the males incubate them. A second clutch is laid that the female incubates herself.

Polyandry in Northern Jacana^[17]

In Polyandry, one female mates with multiple males (and one male only mates with one female) and is a unique mating system which occurs in less than 1% of all bird species. Parental roles are reversed and cause males to provide most of the care given to offspring. Parental roles also cause a reverse in phenotypic differentiation (genetics) resulting in more colorful and larger females compared with males.

Two main types of polyandry exist: simultaneous polyandry and sequential polyandry. An even rarer subtype called cooperative simultaneous polyandry also exists in some species.

In simultaneous polyandry, the female will dominate a certain territory that contains several small nests with two or more males who take care of the offspring. Parental roles are unique since females compete for the males who do most of the parental care work. The Northern jacanas actively practice this in regions such as Southern United States and from Mexico to Panama.

The females will mate with the males in the territory often on the same day. In return, the females will help defend the territory. No copulation occurs during the incubation period and during the first six weeks after the offspring is hatched. If something happens to the eggs, the female will mate with the male once again. This can lead to competition in some species.

In cooperative simultaneous polyandry, multiple males mate with a single female and a clutch of mixed eggs (belonging to multiple males) are cared for by the whole group. Species that exhibit this behavior include certain types of Acorn Woodpeckers and Harris Hawks.

In sequential polyandry (the most common form of polyandry) a female mates with a male and lays her eggs. This female then leaves leaving the male to care for the clutch while she repeats the process with another male. Species that exhibit this behavior include certain types of red and red-necked phalaropes, and spotted sandpipers which breed in South Africa. (Paul R. Ehrlich, David S. Dobkin, and Darryl Wheye)^[18]

Factors affecting parental care

Ecological conditions

The male to female ratio has an effect on the type and amount of care provided. With an increase in available mates in some birds (such as the rock sparrow), female desertion rate increases leading to more mono-parental care. When female rock sparrows were exposed to an abundant amount of male mates approximately 50% of the females deserted their first nest when the hatchlings were on average 14.3 days old. The fathers successfully took over all parental duties (Pilastro).^[12]

Female birds can predetermine the sex of their chicks

Female birds are able to produce more of a certain gender of birds that are more likely to survive under extreme conditions. In birds, the females' egg determines the gender of the offspring, not the male's sperm. In zebra finches, a study showed the effect of food on gender ratio production. For females, egg production is a metabolically exhausting and nourishment draining process. It was found that the sex of an egg right after it has been laid and the amount of nutrients made available to a growing embryo can be determined as well. Bigger eggs mean bigger young that have a higher survivability rate.^[19]
In a study of zebra finches, it was determined that those who were fed a lower quality diet laid eggs that were lighter and less nutrient rich than those zebra finches who were fed a higher quality diet. Therefore, those fed a lower quality diet produced more sons and those fed high quality produced more daughters (bigger, more nutrient-rich eggs) because in nature female offspring need more nourishment than males to survive and grow. Males need less nourishment because they do not lay eggs. Since zebra finches can increase the survivability rate of their species, this can be seen as a pre-birth parental care adaptation. (Nicholas B. Davies)^[20]

Timing and temperature (homeothermy) of reproduction

A known trend shows that most birds reproduce earlier if spring comes early with high temperatures. Climate change makes it difficult to notice a connection between temperature and the time of reproduction. Visser et al. (2009) has attempted to find this connection with a 6-year-long experiment in great tits (Parus major). If spring comes three weeks early, birds are more likely to reproduce quicker. This act is caused by early implementation of ornamental cues. He found this to be a fact in both wild and captive birds. Higher early spring temperatures also leads to higher level of parental care given to offspring because of more commitment and less chance of desertion from both parents. Since, parents find mates to reproduce earlier this can be seen as a pre-birth parental care adaptation because of less desertion.^[12]

Benefits and costs of parental care

Parental investment is any form of investment made by a parent that increases an offspring's rate of survival (reproductive success) at the expense of the parent or parent's ability to divert investment towards a new brood. The cost must yield sufficient benefits to ensure current and future breed survival. If parents invest too much parental care into the current brood their future brood will be at risk or cease to exist entirely. An ideal level of parental investment that will ensure the survival and optimal quality of both broods exists. David Lack (1958)^[21]

The brood size (number of eggs laid per clutch) is another factor which effects quality and survival rate. To increase reproductive success over a mate's lifetime a parent must spread parental investment effectively between a current and a future brood. G.C. Williams (1966)^[22]

If there is a higher level of feeding in birds such as the collared flycatchers (Ficedula albicollis), then there is an increase in parental investment during the mating season. However the reproductive success of the future brood will decrease. (Gustafsson & Sutherland, 1988) The cause might be that effort reserved for reproduction is diminished by a need to maintain the immune system this leads to a physiological condition hindering breeding. (Sheldon & Verhulst, 1996; Norris & Evans, 2000)

In most bird species, females invest in parental care more than males at the expense of reproductive success. If both parents contribute to young feeding and guarding at the same rate, the parents reproductive success increases while together. Desertion by any mate would be a setback because parental investment would be diverted to finding a new mate. A male often deserts first because internal fertilization allows the male to impregnate and leave. Males rely heavily on the quantity of offspring for reproductive success.

A hypothesis was tested in South America to see if species of birds would respond more aggressively to an adult predator (a hawk) than their Northern counterparts because they care more about future reproductive success due to a smaller brood size. On the other hand, those in North America respond more aggressively to an offspring predator (a jay) because they care more about their current brood due to a larger brood size. (Cameron Ghalambor and Thomas Martin (2001))

Often parents change the level of parental care provided to manage the cost and benefits of parental care. Passerine species in North America have a large brood size containing 4–6 offspring and a 50% adult survival rate, and those in South America have a smaller brood size containing 2–3 offspring and a 75% adult survival rate. An increase in parental investment (shown by the number of trips made) also increases the threat of predation. The number of visits decreased in the presence of predators of adult birds and predators of offspring was noted in 5 species of birds in the same study. A comparison was made between the same species in the North and South (bunting, thrush, warbler, flycatcher and the wren).

Parents can also vary parental investment to meet a current brood requirements. In 2011, the hihi (Notiomystis cincta) species were fed a sugary solution to make their mouths redder. Redder mouths acted as an ornamental cue signaling healthier offspring for a potential mate. The experiment showed that those fed the sugary solution had an increased chance to create an additional future clutch during the same mating season. (Rose Thorogood and colleagues (2011))^[23]

Evolutionary advantages

Offspring quantity is boosted by weaker birds who release steroids

A lesser black-backed gull^[24]

In black-backed gulls (Larus fuscus) female gulls who exist in poor conditions would usually give their chicks steroids causing a higher survival rate in them. By comparing the level of androgens with a control group, it was found that females who were treated to have a better body condition produced eggs with a lower level of androgens (such as testosterone). (Verboven et al. (2003)) This shows that females with a lower body condition (which correlates with poor conditions) give their chicks a steroid boost so that they have a better chance at survival. This contradicts with Verboven's original hypothesis that gulls in better condition would produce these steroids. Black-backed gulls give these androgens to their chicks via egg formation in the yolk. (Verboven et al. (2003)) Steroids offer equal opportunity for Black-backed birds to flourish in ideal and hostile conditions and serve as a pre-birth form of parental care.^[25]

Anatomical and physiological advantages

Upon closer observation of the yolk in some bird eggs antibodies of mostly IgY (or IgG). The growing bird fetus uses up the yolk which contains IgY. Upon hatching, the young chick starts to create his own IgY but the mothers antibodies will still influence development and growth rate. This IgY is extremely important to avoid problems occurring from a depressed immune system. In case of surgical bursectomy of a mother bird the helper T cells which normally attack pathogens become depressed. The young birds are at risk of disease and may have a lower survival rate depending on environmental conditions (Grindstaff 2003).^[26]
Carotenoids in egg yolk are responsible for the red or yellow color. They protect the underlying fetus's tissues from the free radicals in the environment. Protection against damage caused by lipids in birds is enhanced by vitamin E and other antioxidants that are infused with the carotenoids and yolk. These same antioxidants also prevent the destruction of maternal antibodies (IgY) which are extremely important to survival rate and can be seen as a form of pre-birth parental care. (Grindstaff)^[27]

Methods of providing care

Iberian rock sparrows

There is a clear distinction between the roles of both parents in the Iberian rock sparrows. The female incubates the eggs 11–14 days before they hatch. Then, the female feeds the offspring while the male teaches them to fly and leave the nest usually within only 18 days of birth. The male also feeds the offspring a little less than half the time, easing the burden on both parents. Rock sparrows mostly bring one food item per trip and other times guard the nest. It was commonly observed how this species comes to the nest to guard their young when they are not bringing food, often as a prevention tactic to scare off predators. Rock sparrows raise their heads to display their yellow patch and make a noise when guarding. (Rikón, Amanda Garcia Del)^[12][28]

Shorebirds

Shorebirds chicks are precocial with parents who offer low parental investment, but still fulfill offspring requirements through collaborated polygamy. Future reproductive success is dependent on changes in parental investment, where low investment results in higher mating opportunities and high investment results in lower mating opportunities (lower future reproductive success). The sexual conflict hypothesis fits both results more than the parental investment hypothesis. (Gavin H. Thomas, Tamás Székely)^[29]

Correlation between ornamental cues and parental care

Iberian rock sparrows (Petronia petronia)

There is a positive correlation between ornamental cues and the parental care invested in Iberian rock sparrows (Vincente Garcia-Navas). Males show more parental effort if their female mate has a larger yellow chest patch. Also, larger nestlings belonged to those who had males with larger yellow chest patches. There is also a connection between a larger yellow breast patch and higher parental effort but only from the males. Males who mated with females with a bigger yellow chest had a higher rate of visiting their offspring. Bigger males bred later and fed their young more than their smaller counterparts. Larger males are not in a hurry to mate because they are in better condition and can weigh their options. (Rikón, Amanda Garcia Del)^[30]

Common yellowthroats (Geothlypis trichas)

Two pair species of common yellowthroats were analyzed from Wisconsin and New York for the effect of ornamental cues on parental care. Males possess a black face mask and yellow (breast, throat, and belly) patch which is usually completely absent in females. In both U.S. states, yellowthroat males with a larger patch had a lower parental investment towards their young however the ornament involved varied. In Wisconsin males with a larger face mask showed lower parental care and their yellow patch had no effect on parental care. In New York, males with a larger yellow patch showed lower parental care and their larger face mask had no effect on parental care. (Alonzo, Suzanne H.) Females in Wisconsin were not affected by a larger black face mask in providing parental care and likewise females in New York were not affected by yellow patch size, conflicting with the good parent hypothesis (larger ornamental cues lead to higher parental care). The trade-off hypothesis matches the results which says larger ornamental cues on males leads to less parental investment because their effort is diverted to finding more mates for future reproductive success or holding on to territories.^[31]

Ficedula flycatchers

Older male Ficedula flycatchers with large badge sizes had a harder time establishing a territory when compared with those with smaller badge sizes. However, younger males with large badge sizes who got hold of territory provided less parental care (feeding) than those with smaller badge sizes and females. Total parental investment and future reproductive success between both groups of males was unaffected because females adjusted their parental investment to accommodate. Large badge size leads an increase in male to male competition because they divert their parental investment towards showing off their badge during mating. (Anna Qvarnstrõm).^[32]

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