Sexual selection in amphibians

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Male Dendropsophus microcephalus calling Dendropsophus microcephalus - calling male (Cope, 1886).jpg
Male Dendropsophus microcephalus calling

Sexual selection in amphibians involves sexual selection processes in amphibians, including frogs, salamanders and newts. Prolonged breeders, the majority of frog species, have breeding seasons at regular intervals where male-male competition occurs with males arriving at the waters edge first in large number and producing a wide range of vocalizations, with variations in depth of calls the speed of calls [1] and other complex behaviours to attract mates. The fittest males will have the deepest croaks and the best territories, with females making their mate choices at least partly based on the males depth of croaking. This has led to sexual dimorphism, with females being larger than males in 90% of species, males in 10% and males fighting for groups of females.

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There is a direct competition between males to win the attention of the females in salamanders and newts, with elaborate courtship displays to keep the females attention long enough to get her interested in choosing him to mate with. [2] Some species store sperm through long breeding seasons, as the extra time may allow for interactions with rival sperm. [3]

Selection in salamanders

Smooth newt Common Newt.jpg
Smooth newt
Italian crested newt Alpen Kammmolch, Triturus carnifex 7.JPG
Italian crested newt
Red-backed salamander Plethodon cinereus.jpg
Red-backed salamander

Important aspects of courtship displays include male alert posture, approach and pursuit, the marking of the substrate trail, and tail undulations. [2] Once a male has the attention of the female, he may release pheromones, which are used for individual recognition, mate recognition, and mate choice decisions, [4] and generally increase female receptivity towards the male's spermatophore and improve his chances of reproductive success with her. In the red-legged salamander (Plethodon shermani), males directly apply pheromones onto the female's nares. [5] In the aquatic smooth newt (Lissotriton vulgaris), the pheromones are delivered indirectly; the male wafts them towards the female with his tail. [6] In some species, it has been shown that the size a larger, more elaborate male's tail has played a role in the female's decision to mate. [7] In the newt species of the Italian crested newt (Triturus carnifex), males that possessed large mid-dorsal body crests were more favorable to the females looking to mate. [8]

Female choice is the final step in the males attempt to reproduce; if the female does not find the male's traits desirable, reproduction will not be successful. As it is in most species, body size is an important and most common desired trait amongst females. Body size is indicative of fitness and/or genetic quality; and because it is easily observable, it can be an indicator for how a female will pick her mate. A larger body size positively correlates to higher paternity; thus larger males are more successful in siring more offspring than smaller males. [9] Male salamanders also prefer larger females because they produce more ova than smaller females. [10]

In sexual coercion, a form of male sexual intimidation which includes forced copulations, repeated mating attempts with the same female, and punishing resisting females. [11] males forcibly mate with females; an example is the red-backed salamander (Plethodon cinereus). It has also been proposed as a third form of sexual selection, along with intersexual selection and intrasexual selection, [11] even though prevailing scientific opinion is that sexual coercion is a manifestation of sexual conflict, stemming out of the natural discord between males and females. In some species of salamanders, females that are territorial and aggressive also intimidate males. Plethodon cinereus females aggressively punish males who are exhibiting social polygyny. [12] Males have been shown to punish females that partake in mating polyandry, forcing them into mating monogamously. [13]

Populations of salamanders tend to be heavily male-biased, which results in a higher number of males vying for access to the lesser number of females. [14] Males will use different tactics in an effort to keep other males away from the female of interest and ensure their own paternity and reproductive success, such as sexual defense, which is used to steal other males spermatophore, which may have already deposited into the female, and sexual interference, when a male pushes the female away from another courting male, [10] such as sperm capping, whereby a competing male lays his spermatophore directly on top of those previously deposited by another male. Females also participate in sexual interference: a rival female places herself between the courting male and the female he is courting, and attempts to engage the male in their own courtship dance, [15] a tactic for avoiding sperm competition. The male removes the sperm from a female who had mated with a previous male: many species of salamanders will remove the spermatophore from the previous male and insert his own; thus, ensuring his paternity. [16] [17]

Sperm storage is a method by which females can control the sperm that fertilizes their eggs. Female salamanders and newts, most notably Triturus vulgaris , possess sperm-storage glands called spermathecae in the walls of their cloacae. [18] Sperm storage has evolved independently to control reproduction in response to the environment. Females have the ability to store multiple spermatophores until they are needed for fertilization. [17] Sperm storage leads to the post-copulatory sexual selection process of cryptic female choice, which occurs when a female removes the deposited sperm or favors one set of spermatophore over another, during or after copulation. [19] Spermatophores are composed of a cap containing the spermatozoa and a gelatinous support arrangement which fastens the spermatophore to a substrate. [20] Spermatophores are very central to reproductive success; therefore, they are handled carefully. Mating success has a direct correlation to favorable phenotypic traits such as tail loss, adult body size, and age. [21]

Vocal signaling in frogs

Gray tree frog Hyla versicolor.jpg
Gray tree frog
Glass frog Hyalinobatrachium fleischmanni01a.jpg
Glass frog
Northern cricket frog Acris crepitansPCCA20061001-8206B1.jpg
Northern cricket frog
Boophis madagascariensis Boophis madagascariensis01.jpg
Boophis madagascariensis

The vocalizations that male frogs use to call for females are crucial for reproductive success in frogs. [22] Initially, male frogs produce advertisement calls, considered a pre-mating isolating mechanism because females use them to isolate conspecific males, [23] as cited in [24] which convey information about species, sexual readiness, and size, [24] with females moving towards the call they find most attractive. In Hyla versicolor , females favor long calls rather than short calls [25] while in Dendropsophus microcephalus they are attracted to short and high rate calling. [24]

isolated spring peeper call.

If a female shows interest male frogs will switch to courtship calls, [24] some of which are simply an increase in rate, [23] as cited by Wells and Schwartz, [24] which can contain fifty percent more notes than advertisement calls, and can become more complex when a male is at a specific oviposition site. [26] as cited by [24] The glass frog ( Hyalinobatrachium fleischmanni ) from Panama gives long calls when a female frog is first seen and will switch to multiple staccato chirps once a female indicates interest. [27] as cited by [24]

Since anurans are highly sensitive to motion, females use conspicuous movements to communicate interest. [28] A female frog may also send vocal signals of her own to males, motivating copulation and competitive behaviors. [29] Female Iberian midwife toads (Alytes cisternasii) use courtship calls to distinguish themselves from other male competitors. The African common platanna ( Xenopus laevis ) uses duet calling when males are not visible, allowing females to distinguish territorial males from satellite males. [30] The Emei music frog (Babina daunchina) female calling stimulates male movement towards sound or phonotaxis.

sophisticated call of Brazilian Torrent Frog.

Calling is an energetically expensive activity, requiring high levels of aerobic respiration. Selection favors the most efficient call production, a good quality call that does not require high levels of energy. [24] allowing a male frog to be able to call continuously for females. Dendropsophus microcephalus , a small tree frog, will produce 100 notes per minute for several hours, requiring up to 25 times more oxygen. [24] Some frogs produce less energetic calls and remain in chorus for longer periods of time with the ability to remain active longer being better for mating success than a higher energy vocal display. [25]

The morphological and biochemical processes of call production are influenced by sexual selection. [23] as cited by [24] Male frogs have developed vocal sacs that enable louder calls, with the larger tympanum increasing the radiation of the vocal signal. [31] as cited by [32] Males also have larger trunk muscles with highly aerobic muscle fibers, many mitochondria, and fat storage. [25]

The sensory exploitation hypothesis states that females have natural preexisting preferences for sexual signals that have been favored by sexual selection, [33] with males producing calls that are known to be favorable for females. A recent study of advertisement calls from 72 species of anurans has indicated that most call features in males show phylogenetic correlation, indicating that species-specific evolution of calls might be constrained by a lack of genetic variation or because female preferences for call features have diverged to only a limited extent. [34] Male anurans will often alter the rate of calling in order to intimidate other males though females tend to favor advertisement and courtship calls over aggressive ones, indicating that aggressive vocalizations are a form of male- male competition. [35] as cited by [24]

Advertisement and aggressive calls are usually similar in frequency but produced at different rates. Geocrinia victoriana , an eastern Australian smooth frog, has a long aggressive note to ward off competitors and shorter notes to attract females. [36] In Northern cricket frogs (Acris crepitans) male aggressive calls serve a dual purpose of attracting females and intimidating other male callers. The Madagascar bright eyed frog ( Boophis madagascariensis ) is able to produce 28 different types of aggressive calls by modifying pulse rate and notes. [37] as cited by [24]

Males can intercept vocal signals that were not meant for them in a tactic known as eavesdropping. The Hyla versicolor male increases calling rate and duration once a female is in vicinity. Eavesdroppers will intercept these increased signals and begin to call for the female in a more aggressive manner, [24] which generally leads to escalated conflicts. [38] [39] Eavesdropping also allows male frogs to assess the body size of their competitors. [24] The frequency of vocal signals is dependent on the mass of the laryngeal apparatus, and a large one will produce lower frequency calls, positively correlated to overall body size. [39] Male frogs will use eavesdropping to decide whether or not to initiate aggressive conflicts. Male anurans are more likely to attack a frog with higher frequency calls. [39] It can also inform frogs when the competition has become too intense, where it can reduce or stop calling altogether and move to a different location outside of the chorus. In order to save energy they attempt to call females where there is less competition and a better chance to court a female. [24] Once a satellite male hears a change in vocalizations of other males he will begin courtship calling in an attempt to steal a female, with some males now invests more energy into a competitive courtship call which may sway the female's interest. Satellite males may contribute 20% of sexual reproduction in a populations. [40] as cited by [41]

Polygynandry in frogs

Allobates femoralis Allobates femoralis.jpg
Allobates femoralis
Bibron's toadlet Pseudophryne bibronii.jpg
Bibron's toadlet

Anuran mating systems are promiscuous: females and males breed with multiple mates and females exhibit sequential polyandry when one female is fertilized by more than one male at different times. Anurans are external fertilizers so there is no sperm competition. [42] Polyandry has benefits for females such as fertility insurance, paternal care insurance and dispersal of mortality risk. Female anurans have a high risk of mating with sperm depleted males due to frequent mating [42] and tend to select the same few males displaying fitness qualities. The requirement for successful copulation is that the male and female gametes have to be released at the same time and at the right orientation. [43] as cited by [42]

In anurans, 70% of polyandrous species exhibit paternal care. In Allobates femoralis the female's offspring survival depends on the male's carrying abilities, as they are responsible for carrying tadpoles from terrestrial to aquatic sites. [42] If a female only mates with one male and he is a poor parent, she may lose all of her offspring. Females reduce the risk of losing all of their offspring because it is likely that some of the males they mated with make good parents. [42] Sequential polyandry will allow females to have a multiple clutches in different nest sites, reducing the risk of abiotic factors, such as temperature, or biotic factors like predators affecting development of the offspring. [44] as cited by [42]

Some male behaviors that may have led to polyandry are displacement, where a male is gripped onto and mating with a female, another male may make an effort to mate as well and displace the male that was originally copulating; forced copulation, where there is a high density of aggressive males, and female abandonment, where a female but spots a better one to mate with and abandons the less favorable one. This can lead to sequential polyandry if the male leaves before the entire clutch is released and an additional male fertilizes these eggs as well. [42] In Bibron's toadlet (Pseudophryne bibronii), females spread out their eggs across the nests of two to eight males, with those who exhibited higher levels of polyandrous behavior having higher mean offspring survivorship, showing that insurance against nest failure and dispersal of mortality risk is related to the evolution of polyandry. [45]

Dimorphism and morphology

Small male and large female Fleay's barred frog (Mixophyes fleayi) in amplexus Mixophyes fleayi01.jpg
Small male and large female Fleay's barred frog (Mixophyes fleayi) in amplexus
Male tusked frog Adelotus brevis.jpg
Male tusked frog

Sexual dimorphism is seen as size difference between sexes in salamanders [46] and in 90% of anuran species. [47] Larger females is a result of selection for fecundity, including egg size or clutch size as they can store more energy and produce more offspring. [48] as cited by [41] Females are never more than twice the size of males. [41]

Size is important in male-male competition, with larger males having an advantage, due to the "male combat hypothesis" [47] which suggests that male combative behavior is positively related to male body size. Males in the tusked frog (Adelotus brevis) and the fanged frog (Limnonectes kuhlii) use fangs and tusks as weapons to defend their calling sites. Larger body size and larger weaponry leads to higher reproductive rates. [49] as cited by [41] However, data suggest that this male mechanism only operates in superfamily Dentrobatoidea, [41] possibly due to alternative mating techniques that reduce selection pressure on body size. Large African bullfrog ( Pyxicephalus adspersus ) males defend territories while small intimidated males move away and become satellite males. These smaller males use eavesdropping techniques and mate with females who are in range of their satellite location. [41]

Sexual role reversal in Dendrobates auratus

Poison dart frog Dendrobates auratus Dendrobates auratus, poison dart frog.jpg
Poison dart frog Dendrobates auratus

Initial observation of mating in the green poison-dart frog Dendrobates auratus shows convincing evidence of sex-role reversal. Small female clutch size, female-female competition, and large parental care investment by males are characteristic of sexual role reversal. [50] as cited by [51] To test whether this sexual role reversal was true, two hypotheses were tested; the sexual role reversal hypothesis and the parental quality hypothesis. [52]

For the sexual role reversal hypothesis to be true, females would compete for as many males as possible, and this was not supported because male-male competition for mates was as common as female-female competition. In sexual role reversal males usually become more selective; however, in Dendrobates auratus females were more selective when choosing males, supporting the parental quality hypothesis, which predicted that females would compete for the parental care of particular males. Females were defensive of their mating partners and used courtship techniques to prevent males from mating with other females and destroyed rivals' eggs. [52] These observations support the parental quality hypothesis. Summers [52] weakens the sexual role reversal hypothesis and strengthens the case parental quality selection.

Related Research Articles

<span class="mw-page-title-main">Sexual selection</span> Mode of natural selection involving the choosing of and competition for mates

Sexual selection is a mode of natural selection in which members of one biological sex choose mates of the other sex to mate with, and compete with members of the same sex for access to members of the opposite sex. These two forms of selection mean that some individuals have greater reproductive success than others within a population, for example because they are more attractive or prefer more attractive partners to produce offspring. Successful males benefit from frequent mating and monopolizing access to one or more fertile females. Females can maximise the return on the energy they invest in reproduction by selecting and mating with the best males.

<span class="mw-page-title-main">Amplexus</span> Type of mating behavior exhibited by some externally fertilizing species

Amplexus is a type of mating behavior exhibited by some externally fertilizing species in which a male grasps a female with his front legs as part of the mating process, and at the same time or with some time delay, he fertilizes the eggs, as they are released from the female's body. In amphibians, females may be grasped by the head, waist, or armpits, and the type of amplexus is characteristic of some taxonomic groups.

<span class="mw-page-title-main">Plethodontidae</span> Family of amphibians

Plethodontidae, or lungless salamanders, are a family of salamanders. Most species are native to the Western Hemisphere, from British Columbia to Brazil, although a few species are found in Sardinia, mainland Europe south of the Alps, and South Korea. In terms of number of species, they are by far the largest group of salamanders.

The Coolidge effect is a biological phenomenon seen in animals, whereby males exhibit renewed sexual interest whenever a new female is introduced, even after sex with prior but still available sexual partners. To a lesser extent, the effect is also seen among females with regard to their mates.

<span class="mw-page-title-main">Spermatophore</span> Packet containing sperm in invertebrate reproduction

A spermatophore or sperm ampulla is a capsule or mass containing spermatozoa created by males of various animal species, especially salamanders and arthropods, and transferred in entirety to the female's ovipore during reproduction. Spermatophores may additionally contain nourishment for the female, in which case it is called a nuptial gift, as in the instance of bush crickets. In the case of the toxic moth Utetheisa ornatrix, the spermatophore includes sperm, nutrients, and pyrrolizidine alkaloids which prevent predation because it is poisonous to most organisms. However, in some species such as the Edith's checkerspot butterfly, the "gift" provides little nutrient value. The weight of the spermatophore transferred at mating has little effect on female reproductive output.

<span class="mw-page-title-main">Internal fertilization</span> Union of an egg and sperm to form a zygote within the female body

Internal fertilization is the union of an egg and sperm cell during sexual reproduction inside the female body. Internal fertilization, unlike its counterpart, external fertilization, brings more control to the female with reproduction. For internal fertilization to happen there needs to be a method for the male to introduce the sperm into the female's reproductive tract.

External fertilization is a mode of reproduction in which a male organism's sperm fertilizes a female organism's egg outside of the female's body. It is contrasted with internal fertilization, in which sperm are introduced via insemination and then combine with an egg inside the body of a female organism. External fertilization typically occurs in water or a moist area to facilitate the movement of sperm to the egg. The release of eggs and sperm into the water is known as spawning. In motile species, spawning females often travel to a suitable location to release their eggs.

<span class="mw-page-title-main">Sexual conflict</span> Term in evolutionary biology

Sexual conflict or sexual antagonism occurs when the two sexes have conflicting optimal fitness strategies concerning reproduction, particularly over the mode and frequency of mating, potentially leading to an evolutionary arms race between males and females. In one example, males may benefit from multiple matings, while multiple matings may harm or endanger females, due to the anatomical differences of that species. Sexual conflict underlies the evolutionary distinction between male and female.

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Teleogryllus oceanicus, commonly known as the Australian, Pacific or oceanic field cricket, is a cricket found across Oceania and in coastal Australia from Carnarvon in Western Australia and Rockhampton in north-east Queensland

<span class="mw-page-title-main">Sexual cannibalism</span> Practice of animals eating their own mating partners

Sexual cannibalism is when an animal, usually the female, cannibalizes its mate prior to, during, or after copulation. It is a trait observed in many arachnid orders and several insect and crustacean clades. Several hypotheses to explain this seemingly paradoxical behavior have been proposed. The adaptive foraging hypothesis, aggressive spillover hypothesis and mistaken identity hypothesis are among the proposed hypotheses to explain how sexual cannibalism evolved. This behavior is believed to have evolved as a manifestation of sexual conflict, occurring when the reproductive interests of males and females differ. In many species that exhibit sexual cannibalism, the female consumes the male upon detection. Females of cannibalistic species are generally hostile and unwilling to mate; thus many males of these species have developed adaptive behaviors to counteract female aggression.

<span class="mw-page-title-main">Ocoee salamander</span> Species of amphibian

The ocoee salamander is a species of salamander in the family Plethodontidae. This salamander has a variety of colors and patterns, and got its name from Tennessee state wildflower. Its natural habitats are temperate forests, rivers, intermittent rivers, freshwater springs and wet rocks in mountainous areas of the Southeastern United States. It was first described by Nicholls in 1949. They are territorial and feed on small invertebrates. It is widely distributed in the southeastern United States and is listed as "Least Concern" by the International Union for Conservation of Nature.

<span class="mw-page-title-main">Courtship display</span> Communication to start a relationship with someone or to get sexual contact

A courtship display is a set of display behaviors in which an animal, usually a male, attempts to attract a mate; the mate exercises choice, so sexual selection acts on the display. These behaviors often include ritualized movement ("dances"), vocalizations, mechanical sound production, or displays of beauty, strength, or agonistic ability.

<i>Utetheisa ornatrix</i> Species of moth

Utetheisa ornatrix, also called the ornate bella moth, ornate moth, bella moth or rattlebox moth is a moth of the subfamily Arctiinae. It is aposematically colored ranging from pink, red, orange and yellow to white coloration with black markings arranged in varying patterns on its wings. It has a wingspan of 33–46 mm. Moths reside in temperate midwestern and eastern North America as well as throughout Mexico and other parts of Central America. Unlike most moths, the bella moth is diurnal. Formerly, the bella moth or beautiful utetheisa of temperate eastern North America was separated as Utetheisa bella. Now it is united with the bella moth in Utetheisa ornatrix.

Interlocus sexual conflict is a type of sexual conflict that occurs through the interaction of a set of antagonistic alleles at two or more different loci, or the location of a gene on a chromosome, in males and females, resulting in the deviation of either or both sexes from the fitness optima for the traits. A co-evolutionary arms race is established between the sexes in which either sex evolves a set of antagonistic adaptations that is detrimental to the fitness of the other sex. The potential for reproductive success in one organism is strengthened while the fitness of the opposite sex is weakened. Interlocus sexual conflict can arise due to aspects of male–female interactions such as mating frequency, fertilization, relative parental effort, female remating behavior, and female reproductive rate.

A nuptial gift is a nutritional gift given by one partner in some animals' sexual reproduction practices.

<span class="mw-page-title-main">Sexual selection in birds</span>

Sexual selection in birds concerns how birds have evolved a variety of mating behaviors, with the peacock tail being perhaps the most famous example of sexual selection and the Fisherian runaway. Commonly occurring sexual dimorphisms such as size and color differences are energetically costly attributes that signal competitive breeding situations. Many types of avian sexual selection have been identified; intersexual selection, also known as female choice; and intrasexual competition, where individuals of the more abundant sex compete with each other for the privilege to mate. Sexually selected traits often evolve to become more pronounced in competitive breeding situations until the trait begins to limit the individual's fitness. Conflicts between an individual fitness and signaling adaptations ensure that sexually selected ornaments such as plumage coloration and courtship behavior are "honest" traits. Signals must be costly to ensure that only good-quality individuals can present these exaggerated sexual ornaments and behaviors.

<span class="mw-page-title-main">Sexual selection in mammals</span> Mode of natural selection

Sexual selection in mammals is a process the study of which started with Charles Darwin's observations concerning sexual selection, including sexual selection in humans, and in other mammals, consisting of male–male competition and mate choice that mold the development of future phenotypes in a population for a given species.

<span class="mw-page-title-main">Sexual selection in scaled reptiles</span>

Sexual selection in scaled reptiles studies how sexual selection manifests in snakes and lizards, which constitute the order Squamata of reptiles. Each of the over three thousand snakes use different tactics in acquiring mates. Ritual combat between males for the females they want to mate with includes topping, a behavior exhibited by most viperids in which one male will twist around the vertically elevated fore body of its opponent and forcing it downward. It is common for neck biting to occur while the snakes are entwined.

<span class="mw-page-title-main">Mating of gastropods</span>

The mating of gastropods is a vast and varied topic, because the taxonomic class Gastropoda is very large and diverse, a group comprising sea snails and sea slugs, freshwater snails and land snails and slugs. Gastropods are second only to the class Insecta in terms of total number of species. Some gastropods have separate sexes, others are hermaphroditic. Some hermaphroditic groups have simultaneous hermaphroditism, whereas some sequential hermaphroditism. In addition, numerous very different mating strategies are used within different taxa.

<span class="mw-page-title-main">Polyandry in animals</span> Class of mating system in non-human species

In behavioral ecology, polyandry is a class of mating system where one female mates with several males in a breeding season. Polyandry is often compared to the polygyny system based on the cost and benefits incurred by members of each sex. Polygyny is where one male mates with several females in a breeding season . A common example of polyandrous mating can be found in the field cricket of the invertebrate order Orthoptera. Polyandrous behavior is also prominent in many other insect species, including the red flour beetle and the species of spider Stegodyphus lineatus. Polyandry also occurs in some primates such as marmosets, mammal groups, the marsupial genus' Antechinus and bandicoots, around 1% of all bird species, such as jacanas and dunnocks, insects such as honeybees, and fish such as pipefish.

References

  1. ↑ Tungara Frog Study’s Findings Counter Sexual Selection Theory Published 29 August 2015, by Matt Towns
  2. 1 2 Romano, Antonio; Giacomo Bruni (2011). "Courtship behaviour, mating season and male sexual interference in Salamandrina perspicillata". Amphibia-Reptilia. 32 (1): 63–76. doi: 10.1163/017353710X541878 .
  3. ↑ Adams, Erika M.; Jones, A.G.; Arnold, S.J. (2005). "Multiple paternity in a natural population of a salamander with long-term sperm storage". Molecular Ecology. 14 (6): 1803–1810. doi:10.1111/j.1365-294X.2005.02539.x. PMID   15836651. S2CID   18899524.
  4. ↑ Steinfartz, Sebastian; Barbara Caspers (2011). "Preference for the other sex: Olfactory sex recognition in terrestrial fire salamanders (Salamandra salamandra)". Amphibia-Reptilia. 32 (4): 503–508. doi: 10.1163/156853811x603265 .
  5. ↑ M. Kiemnec-Tyburczy, Karen; Sarah K. Woodley; Pamela W. Feldhoff; Richard C. Feldhoff; Lynne D. Houck (2011). "Dermal application of courtship pheromones does not influence receptivity in female red-legged salamanders (Plethodon shermani)". Journal of Herpetology. 45 (2): 169–173. doi:10.1670/10-014.1. S2CID   83886115.
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  10. 1 2 Williams, Rod N.; J. Andrew DeWoody (2009). "Reproductive Success and Sexual Selection in Wild Eastern Tiger Salamanders (Ambystoma t. tigrinum)". Evolutionary Biology. 36 (2): 201–213. doi:10.1007/s11692-009-9058-7. S2CID   22305575.
  11. 1 2 Hucko, Jeffery A.; Jaeger, Robert G.; Prosen, Ethan D (2006). "Sexual coercion in the salamander Plethodon cinereus: is it merely a result of familiarity?". Herpetologica. 62 (1): 10–19. doi:10.1655/04-05.1. S2CID   85816435.
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