Superfetation Mammals

Biol. Rev. (2011), 86, pp. 77–95.
77
doi: 10.1111/j.1469-185X.2010.00135.x
The concept of superfetation: a critical review

on a ‘myth’ in mammalian reproduction
Kathleen Roellig†,∗ , Brandon R. Menzies† , Thomas B. Hildebrandt and Frank Goeritz
Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany
(Received 26 May 2009; revised 10 March 2010; accepted 16 March 2010)
ABSTRACT
Superfetation is understood as another conception during an already ongoing pregnancy. This implies the existence
of young of different developmental stages within the female reproductive tract during certain periods of pregnancy.
Nevertheless, a clear definition of the term as well as distinct criteria to identify the occurrence of superfetation in a species
is missing. The variable anatomy of mammalian reproductive tracts seems to make the occurrence of superfetation more
or less likely but impedes the simple evaluation of whether it is present or not. Additionally, adequate determination
methods are missing or are difficult to apply at the right time. Superfetation or rather superfetation-like pregnancies
are reported for numerous species including humans, livestock and rodents. The usual criteria to assume a case of
superfetation include the finding of discordantly developed young within the uterus during post mortem or parturition
of young after a birth interval shorter than the assumed pregnancy length. Often the occurrence of superfetation is
concluded because other explanations of reproductive artifacts are missing. Even severe reproductive pathologies are
often confused with superfetation. True superfetation or superfetation as a reproductive strategy may exist in some
mammals. In the American mink (Neovison (Mustela) vison) and the European badger (Meles meles) superfetation occurs
in combination with embryonic diapause. In the European brown hare (Lepus europaeus), superfetation has long been
assumed to exist but evidence is still controversial. Superfetation definitely occurs in certain species of poeciliid and
zenarchopterid fish, some of which also exhibit viviparity and maternal care. In mammals, the evolution of such a
reproductive mechanism poses many interesting evolutionary, endocrine, microbial and immunological questions that
require further investigation.
Here we review the scant and at times ancient literature on this poorly understood topic. The different manifestations
of superfetation are defined and reliable criteria to detect superfetation are outlined. Also, the differentiation of
superfetation into a reproductive strategy or as a disrupted, abnormal reproductive function is discussed. Due to the
different discussed functional aspects of superfetation, it is appropriate to establish a more detailed scheme to classify
the true natural superfetation cases into superfertilization, superconception and superfetation proper. To date, there is
no mammal species known for which superfetation proper in terms of finding discordantly developed fetuses has been
conclusively demonstrated to be not only a rare occurence but an evolved reproductive strategy.
Key words: reproduction, superfetation, evolutionary adaptation, superfecundation, reproductive strategy, Eutheria,
Lepus, Neovison, Mammalia, pregnancy.
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 78
II. Theoretical prerequisites for the occurrence of superfetation in mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
(1) Ovulation must be triggered during pregnancy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
(2) Semen must be at the place of fertilization in the oviduct . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
(3) The endometrium must be able to accept blastocysts to start implantation . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
* Address for correspondence: (Tel: +49-30-5168 242; E-mail: kathleen roellig@gmx.de, roellig@izw-berlin.de).
† Both authors contributed equally to this manuscript.
Biological Reviews 86 (2011) 77–95 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society
78 Kathleen Roellig and others
III. Clarification of reproductive phenomena often mistaken for superfetation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82

(1) Superfecundation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
(2) Delayed nidation or diapause . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
(3) Variable pregnancy length . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82
(4) Developmental retardation, embryonic death and resorption . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
(5) Conception during a pregnancy in retrogression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
(6) Split parturition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
IV. Evidence for superfetation in mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
(1) Reproductive modes in mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
(2) Domesticated species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
(3) Laboratory species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83
(4) Wildlife . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 84
(5) Humans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
V. True superfetation in mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
(1) The American mink . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
(2) The European badger . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
(3) The European brown hare . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
(4) Macropodid marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
VI. Superfetation in non-mammalian vertebrates . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
VII. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90
VIII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90
IX. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92
X. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92
I. INTRODUCTION from marsupials to man (Table 1). These reports seldom

distinguish between SF as basic reproductive function, rare
‘‘The hare is often troubled with superfetation’’ (Lovell, occurrence or even pathologic observation, emphasizing
1661). This early scientific description of the phenomenon problems with the definition and clear distinction of SF.
was written by the English naturalist Robert Lovell. The term ‘‘superfetation’’ comes from the latin word
However, one can find disparate references to superfetation ‘‘superfetatio’’ (super = over; fetus, fetura = to fertilize, fertile,
(SF) dating back as far as antiquity to Hippocrates, Herodot, offspring) of which the literal meaning is something
Plinius and Aristotle. ‘‘The hare is an example of this. This like ‘‘overconception’’ or ‘‘supergravidity’’. Based on the
is an animal in which superfetation occurs, for. . .often some meaning of the word, the reproductive condition refers
of its offspring are imperfect; others of its offspring, however, to another fertilization taking place during an ongoing,
intact pregnancy. In general, SF should be defined as
it brings to birth in a perfected state’’ (Aristotle; translation
ovulation, fertilization, and implantation of a second set
by Goold, 1979). It is not completely clear on what basis
of ova during pregnancy (Rollhäuser, 1949). However, this
Aristotle concluded the existence of SF in the hare. However,
very basic definition provides considerable ambiguity when
it is generally thought that he was observing one healthy fetus
trying to characterize the diverse reproductive strategies of
with another in the process of being resorbed by the mother,
mammals. As a result, the assumption of SF in a particular
another aspect of hare pregnancy that makes reproduction species is often based not on observations but rather on
in this species particularly complex. Aristotle also considered deductions. As clear observations of the initial conditions
the condition of SF to be possible in humans. Nevertheless, are demanding, the term SF has been used to mean the
it can be questioned if the term ‘‘superfetation’’ was always bearing of litters at different developmental stages within
used for the same reproductive condition, as knowledge the uterus. However, the finding of discordantly developed
about reproductive functions was limited. offspring inside the uterus does not necessarily imply SF. For
One of the first clear definitions for SF comes from Kuss- SF to take place, ovulation followed by fertilization of oocytes
maul, ‘‘the Hippocrates of the 19th Century’’, which seems from different ovulation cycles must occur. This allows for
to be the basic reference for the definition of SF to date further conception/s during established pregnancy/ies. To
(Kussmaul, 1859). He termed further conceptions after the clarify the distinction between SF and other reproductive
fertilization of an oozyte in a female ‘‘superimpregnation’’. phenomena it is therefore important to evaluate clearly
Furthermore, he clearly separated between further fertiliza- whether a new ovulation and fertilization have taken place
tions within the first menstrual cycle of a pregnancy, calling during an ongoing and intact pregnancy.
this ‘‘superfecundation’’, and further fertilizations in different Nevertheless, this definition still allows misinterpretation.
menstrual or ovulation cycles, terming this ‘‘superfetation’’. For example, Hollander (1960) referred to SF as the
There now exist numerous reports of SF in a wide fertilization of ova from successive ovulations that then
range of scientific journals and in ten orders of mammals become part of one pregnancy, and stated that it is normal in
The concept of superfetation 79
Table 1. Mammals in which superfetation (SF) has been suggested to occur, the accompanying evidence, references and the number
of additional (Add) references cited in other articles, together with an assessment (Poss) of the likelihood of true (T), artificial (A) or
questionable (?) observations of SF in these species. CL, corpus luteum
Subclass Taxonomic name Evidence for SF References Add Poss

Order
Common name
Eutheria
Primates
Human Homo sapiens sapiens Discordance in fetal size Hartel (1958); Fontana & 7 A
Gilles (1970); Scrimgeour
& Baker (1974); Honore &
Nickerson (1977); Walter
et al. (1975); Milne (1956);
Soudre et al. (1992);
Tuppen et al. (1999);
Harrison et al. (2005);
Baijal et al. (2007)
Common chimpanzee Pan troglodytes ? Friedl (1967, cited in A
Bartikova, 1978)
Patas monkey Erythrocebus patas Discordance in inter-birth Leakey (1969) A
interval relative to
pregnancy length
Rodentia
Chinchilla Chinchilla laniger Discordance in fetal size Gitlin & Adler (1968) ?
European beaver Castor fiber Discordant CLs Zurowski & Doboszynska ?
(1975)
Mouse Mus musculus Blastocyst transfer, Stowell (1941); Littleford & A
pathological examination Gysin (1944); Rollhäuser
(1949); Edwards & Fowler
(1958); Barnett & Munro
(1970)
Musk rat Ondatra zibetica Pathological dissection Stieve (1952); Stieve-Miegel ?
(1955)
Common gundi Ctenodactyles gundi Pre-partum oestrus Gouat (1985) ?
Rat Rattus norvegicus Discordance in fetal size, Yoshinaga (1971); Sparrow 2 A
pathological examination, (1977)
artificial induction
Casiragua Proechimys guairae Pre-partum oestrus Weir (1974) ?
Lagomorpha
European brown hare Lepus europaeus Pre-partum oestrus Hediger (1948) and others T
(see text)
Chiroptera
Greater dog-like bat Peropteryx kappleri Discordant fetal size Rasweiler (1982) ?
Greater false vampire bat Megaderma lyra Discordant fetal size Ramaswami & Anand ?
Kumar (1963)
Indian rufus horseshoe bat Rhinolophus rouxi Discordant fetal size Gopalkrishna & ?
Ramakrishna (1977)
Leschenault’s rousette Rousettus leschenaulti Discordance in fetal size and Karim & Gupta (1986) ?
separate ovarian CLs
Short-tailed fruit bats Carollia spp. Discordant fetal size De Bonilla & Rasweiler ?
(1974)
Carnivora
Badger Meles meles Ovarian cycling during Yamaguchi et al. (2006) and T
diapause others (see text)
Cat Felis catus Discordance in fetal size; Harman (1917); Hunt (1919); 4 A
anatomical capacity for SF Markee & Hinsey (1935);
Hoogeweg & Folkers (1970)
Geoffroy’s cat Leopardus geoffroyi Same as lion Bartikova (1978) ?
Lion Panthera leo Discordance in inter-birth Dathe (1961) ?
interval relative to
pregnancy length
Table 1. (Cont.)
Subclass Taxonomic name Evidence for SF References Add Poss

American mink Neovison (Mustela) vison CLs of different quality and Hansson (1947) and others T
offspring of different (see text)
developmental stages
CLs in both ovaries,
discordance in fetal size
Panther Panthera pardus Pathological dissection Anghi et al. (1978) T
California sea lion Zalophus californianus Multiple births within the Wandrey (1977) ?
normal oestrus length
Perrissodactyla
Burro Equus asinus asinus Discordant CLs, pathological Short (1964) A
dissection
Horse Equus cabbalus Discordant CLs, pathological Arbeiter (1965); Egberts & 6 A
dissection Fontyne (1977)
Artiodactyla
Buffalo Bubalus arnee Multiple births within the Rao et al. (1987) T
Cow Bos primigenius domesticus Embryo transfer, discordance Harman (1919); Nottle 8 A
in fetal size, pathological (1976); Carter (2002)
dissection
Goat Capra hircus Same as sheep Kroon (1829) A
Pig Sus scrofa Cycling and mating during Smith (1927); Nottle (1976); 9 A
pregnancy Larivee (1972)
Sheep Ovis gmelini aries Multiple births within the Matter (1965) A
Ovis orientalis aries Scanlon (1960, 1972) 3
White-tailed deer Odocoileus virginianus Same as sheep Bartmann (1971) A
Afrosoricida
Tail-less tenrec Tenrec ecaudatus Consecutive births without Poduschka (1996) ?
further insemination after
parturition
Proboscidea
Elephant (species not known) Multiple births within the Schiött (1908, cited in ?
normal oestrus length Stieve-Miegel, 1955)
Metatheria
Diprotodontia
Swamp wallaby Wallabia bicolor Pre-partum oestrus, oestrus Calaby & Poole (1971); T
consistently shorter than Paplinska et al. (2006)
pregnancy
the mink but not in the horse. This implies that ova fertilized probably never occurs with cases of suspected SF just as
at a later time essentially catch up developmentally to those logically explained on the basis of variation in the timing
fertilized during previous cycles so that all of the developing of implantation among the same set of fertilized eggs i.e.
young are born at the same time. The main problem in parallel embryonic development is occuring rather than SF.
evaluating such conditions is the lack of application of Knaus (1966) was an outstanding critic of SF, especially in
adequate examination and detection methods as well as clear the European brown hare (Lepus europaeus). He made a list
criteria to distinguish SF from other reproductive events. of systematic reasons that it was not possible and regarded
Discussions of SF have often been emotive with at times the concept of intraperitoneal migration of fertilized ova to
a willingness to accept positive arguments while dismissing be more likely than accepting the data of Bloch et al. (1967)
shortcomings in evidence. By contrast skeptics often question describing fertilization of ova by migration of sperm through
the true circumstances of reports. For example, Kuntz the late-pregnant uterus (Knaus, 1967). SF appears to ‘‘break
(1920) demonstrated in cats the retention of dead fetuses the rules’’ of basic mammalian reproductive biology, and has
inside the uterus for relatively long periods without marked assumed a myth-like status making it particularly difficult to
macroscopic changes in their appearance. Therefore, he study. However, several experimental studies in mice and
concluded that the finding of dead fetuses of different sizes cattle have demonstrated that the application of assisted
should not automatically be linked to SF. Weichert (1942) reproductive technologies (ART) can override several basic
had the opinion that a second conception during pregnancy reproductive mechanisms to produce rare reproductive
conditions, such as SF (Wislocki & Snyder, 1931; Carter, the CLs. In induced ovulators, mating is not only necessary
2002). But the issue remains: does SF occur naturally, or for the delivery of semen but also for triggering ovulation.
is it a pseudo-phenomenon (Littleford & Gysin, 1944). Any In the presence of an active CL it is a point of contention as
species faced with the prospect of SF must be able to to whether copulation can induce ovulation. Therefore, SF
overcome multiple endocrine, microbial and immunological cannot be assumed nor ruled out simply based on observed
barriers to reproduction making reproductive systems that copulations during pregnancy.
exhibit SF especially interesting to study.
This review discusses the general concept of SF in (2) Semen must be at the place of fertilization
mammalian reproduction. The numerous reports are in the oviduct
assessed and new criteria developed to specify SF in any
mammalian species. There are two options to fulfill this requirement, either a
fertile mating during pregnancy or long-term semen storage
in the reproductive tract. Acceptance of mating during
pregnancy is not only known for man but has also been
II. THEORETICAL PREREQUISITES described for example in mice, rats, hamsters, rabbits several
FOR THE OCCURRENCE OF SUPERFETATION primate species and spotted hyenas (Crocuta crocuta) (Crew
IN MAMMALS & Mirskaia, 1930; Krehbiel, 1952; Jones, 2005; East et al.,
2003). However, mating behaviour is not necessarily linked to
Bloch et al. (1967) suggested several biological criteria to oestrus. Krehbiel (1952) described mating during pregnancy
determine the presence of SF in the European brown hare. in golden hamsters, but did not observe separate ovarian
Because these criteria are also valid for other mammalian cycles or SF. The date of mating corresponded with the
reproductive systems, they are clarified and extended below. expected recurrence of oestrus. However, there were no
matings post partum or during lactation. He suggested that
(1) Ovulation must be triggered during pregnancy if SF were to occur in golden hamsters it would require a
series of natural accidents. In other species, a mucus plug
For ovulation to occur during pregnancy, complete follicular within the cervix is thought to prevent the passage of sperm
development and maturation must take place. An ovulation during pregnancy, as in humans and mice (Blickstein, 2003).
during pregnancy is more or less excluded in species that In species, with a bicornuate uterus, alternate pregnancies
have a longer oestrous cycle than the mean pregnancy length. using only one uterine horn may be more prone to SF
Nevertheless, even in species where follicular growth follows (Ottow, 1952; Watzka, 1959). The placenta type might also
a rhythmic pattern shorter than the pregnancy length, the play a role: the shape of the zonary placenta, as seen in
stimulus for an ovulation may not necessarily occur during cats and other carnivores, would make the passage of sperm
pregnancy. It has long been assumed in reproductive biology through the uterus mechanically impossible after successful
that the presence of an active corpus luteum (CL) during implantation. Therefore, SF would only be possible in these
pregnancy impedes follicle growth and ovulation (Ottow, species during the preimplantation period of pregnancy.
1952; Watzka, 1959). As stated by Weir & Rowlands (1973, Even where the type of placentation favours the passage
p. 140) ‘‘These two tissues (CL and placenta) have to be of sperm as in rodents or lagomorphs, it is still not clear
removed completely before reproduction can be repeated in whether semen can traverse the late-pregnant uterus to
any one (mammalian) individual’’. In primates and sheep, reach the oviduct.
the change in the progesterone:oestradiol ratio of the blood The passage of semen through the pregnant uterus
during late pregnancy is thought to be one trigger of the onset represents not only a mechanical problem but also an
of labour (Smith, Mesiano & Mc Grath, 2002). If ovulation immunological and microbiological one. In mammals,
did occur during pregnancy the progesterone:oestradiol ratio insemination results in the transmission of seminal factors
might be so shifted far in advance of the desired birth that act, in the female reproductive tract, to promote sperm
date. The enzyme 17β-hydroxysteroid dehydrogenase-2 survival, condition the female’s immune response to tolerate
(17βHSD2) converts the bioactive 17β-oestradiol to the the conceptus and to organize molecular and cellular changes
less active estrone and is upregulated in the endometrium of in the endometrium that facilitate embryo development
the marmoset monkey (Callithrix jacchus) during the secretory and implantation (Robertson, 2005). For example, semen
phase of the ovarian cycle (Husen et al., 2001). The enzyme activates lymphocytes at insemination that may help mediate
17βHSD2 was also found in placental tissue in this animal, maternal tolerance of the conceptus at the implantation site
which might be a mechanism to counteract high oestradiol (Johansson et al., 2004). There is also evidence that seminal
levels and protect the fetus from the onset of parturition. factors influence the timing of ovulation, CL development
Therefore, a spontaneous ovulation during pregnancy is and progesterone synthesis (Robertson, 2007). The seminal
more or less excluded. Nevertheless, it is known that fluid itself contains substances that are capable of inhibiting
horses exhibit spontaneous ovulation during pregnancy as a the fertility of spermatozoa at various stages of the journey
mechanism to establish accessory CLs which then support to the ovum (Shivaji & Bhargava, 1987). These complex
the ongoing pregnancy (Sharp, 1998). The oocytes expelled interactions concerning the uterine passage of sperm are not
here are redundant since the object is the establishment of completely understood in non-pregnant animals. As for the
possibility of semen traversing the pregnant uterus, there are least the demonstration of ovulation and fertilization during
not only functional side-effects but also the risk of transmitting an intact pregnancy and the tracking of the two pregnancies
venereal diseases to the fetus. irrespective of the mechanisms (e.g. sperm storage) that allow
Long-term semen storage would make a fertile mating the phenomenon to occur.
during pregnancy unnecessary. While this strategy is seen
frequently in insects, birds and reptiles where semen can be
stored for periods up to months or years (Licht, 1984;
Shepherd, 1998; Busch & Waberski, 2007), it is not a III. CLARIFICATION OF REPRODUCTIVE
widespread mechanism in mammals. Sperm storage within PHENOMENA OFTEN MISTAKEN FOR
SUPERFETATION
the genital tract of mammals is considered to last from
hours to days (Enders, 1952; Töpfer-Petersen et al., 2003).
The establishment of a female sperm reservoir is due to There are several reproductive conditions in mammals and
adhesion of the spermatozoa to the oviduct epithelium other species that are sometimes confused with SF.
(Töpfer-Petersen et al., 2003; Busch & Waberski, 2007).
In the American mink (Neovison (Mustela) vison), a species (1) Superfecundation
with induced ovulation, mating is known to take place at
least 48 h before ovulation. Therefore, semen must still be Superfecundation is defined as the fertilization by successive
capable of fertilization after this interval (Enders, 1952). matings of oozytes belonging to the same ovulation
In domestic dogs, females are assumed to be capable of cycle, sometimes by different males (multiple paternity)
storing viable semen for up to six days (Busch & Waberski, by contrast with SF which involves the fertilization of
2007). Storage for even longer periods (whole seasons) has oozytes from different ovulation cycles (Kussmaul, 1859;
been demonstrated in bats (Sharifi et al., 2004). But finding King, 1913). Pregnancies with twins or multiples at the
semen within the genital tract during established pregnancy same developmental stage are established and born in
does not necessarily imply its persistence and viability. Also, one litter at the same time. Superfecundation has been
the mechanisms required to ‘‘reactivate’’ stored sperm are shown in several domestic (Starck, 1965) and wild animals
not well understood. Given the paucity of information [Apodemus spp. (Rodentia) (Baker, Makova & Chesser, 1999);
concerning sperm storage in mammals it is possible that snowshoe hare (Lepus americanus) (Burton, 2002); American
SF could occur even without copulation taking place during mink (Yamaguchi et al., 2004); Richardson’s ground squirrel
pregnancy. On the other hand, in induced ovulators, a (Spermophilus franklinii) (Hare, Todd & Untereiner, 2004);
mating (even if not a fertile one) would be required for the European badger (Meles meles) (Dugdale et al., 2007)].
use of stored sperm.
(2) Delayed nidation or diapause
(3) The endometrium must be able to accept Delayed nidation or diapause has been described in nearly
blastocysts to start implantation
100 mammal species and in some, multiple conceptuses at
If one assumes that the finding of different-sized fetuses different developmental stages can be found within one uterus
is caused by SF, then there must have been additional (Renfree & Shaw, 2000). Oocytes (usually from one ovulation
implantations during an ongoing pregnancy. This requires cycle) are fertilized but implanted at different times. Dormant
a certain hormonal environment, probably different from blastocysts can be present in the uterus for varying periods of
the environment in a non-pregnant uterus. Additionally, time depending on the species (days to weeks in some mice
new blastocysts must find an implantation site. Rollhäuser or many years in kangaroos). Delayed nidation often leads to
(1949) stated for mice that implantations are often to be variable pregnancy length because of different time intervals
found at the caudal end of the uterine horn close to the between fertilization and implantation as for example in
cervix. Therefore there might be space at the cranial uterine the American mink (Dukelow, 1966) and roe deer (Capreolus
ends for further implantations. By contrast Bloch (1952) capreolus) (Hermes et al., 2000). Delayed nidation was also
found in mice that implantation seems to occur more or less described as a cause of ‘‘split parturition’’ in the breeding
symmetrically, and called this embryonic spacing. If further pig (Vandeplassche, 1969). This peculiar condition refers to
fertilizations occur during an early stage of pregnancy in different dates of parturition within one litter.
combination with delayed implantation as described for the
American mink (Hansson, 1947), then all of the fertilized
(3) Variable pregnancy length
ova would implant at the same time (see Section V.1). In
the European brown hare, additional conceptions may occur As explained for diapause, different interbirth intervals
shortly before parturition (Bloch et al., 1967; Hediger, 1948; between successive parturitions may not necessarily be due to
Martinet, 1980). Therefore, implantation may not occur SF. However, because a standard gestation length of x days in
until after parturition (see Section V.3). a particular species is often assumed, observed mating prior
In summary, a diagnosis of SF requires thorough to this average number of days often leads to a conclusion
examination of the criteria listed above. We suggest that of fertilization before the last parturition. This conclusion
the clear detection of SF in any species should include at should not be drawn if a species is able to vary the length
of pregnancy and deliver fully developed offspring before and subsequently via the milk (Renfree, 1993). Within
the expiry of the average gestation. In humans, for example, the more diverse subclasses of marsupials and Eutheria,
average pregnancy length is 280 days but can vary between there exist vast differences in reproductive tactics especially
240 and 331 days (Milne, 1956). regarding anatomy, breeding ecology, pregnancy length,
litter size, placentation type and lactation. Each species
(4) Developmental retardation, embryonic death has its own specialized reproductive biology, which, within
and resorption an evolutionary context must be regarded as adapted to
their present niche. When discussing the possibility of SF
During pathological dissections, offspring of different in any mammalian species it is important not only to look
developmental stages can be found inside the uterus with SF at the technical and theoretical possibility of SF, but also
being the obvious conclusion. Yet, it has long been known to understand how it may relate to its general reproductive
that fetuses of polytocous mammals die and are actively strategy.
resorbed by the mother during pregnancy as observed for
example in the rat (Corey, 1933), mouse (Ibsen, 1928),
(2) Domesticated species
pig (Geisert, 1998) and recently in the European brown
hare (Roellig et al., 2005). Kuntz (1920) demonstrated the Many of the potential SF case reports are for domestic
retention of dead fetuses in utero in the cat for extended periods species. Possible examples in livestock include cows, burro,
without substantial macroscopic changes. Furthermore, sheep, pigs and deer (Harman, 1919; Dalrymple & Jenkins,
infectious diseases can be the cause of embryonic death 1951; Short, 1964; Matter, 1965; Bartmann, 1971; Larivee,
and resorption. In pregnant pigs infection with porcine 1972; Scanlon, 1960; Nottle, 1976; Hall, 1987; Hinrichs
parvovirus causes the SMEDI (stillbirth, mummification, & Watson, 1988). SF was also reported in the domestic
embryonic death, infertility)—syndrome, which can spread cat (Harman, 1917; Hunt, 1919; Markee & Hinsey, 1935;
between fetuses (Quinn et al., 1999). In general, it is difficult to Hoogeweg & Folkers, 1970).
establish the true conceptional history in these circumstances. While some of these cases arose after reproductive
In human babies, differences in the development of multiple manipulations such as prostaglandin and equine chorionic
pregnancies can occur with most cases caused by pathological gonadotrophin (eCG) treatment (Egberts & Fontyne, 1977)
circumstances (Blickstein, 2003). others were observed under natural reproductive conditions,
including the birth of viable additional young within the
(5) Conception during a pregnancy in retrogression length of a single oestrous cycle or the discovery of fetuses
of distant developmental age during pathological dissection.
If embryonic death of all conceptuses occurs, it is possible that Such cases may represent true examples of SF (Table 1).
a new pregnancy resulting from a new ovulation cycle may A histological evaluation of two kittens born with a thirteen-
be established. In these cases, newly developing conceptuses day interval revealed both to be fully developed, supporting
may be found alongside more developed but dead ones. In the hypothesis of SF (Markee & Hinsey, 1935). In a buffalo
this case a prerequisite of SF, the fertilization of oocytes from successive mating within a 30-day interval followed by the
different ovulation cycles, would be fulfilled. But there was birth of two 12 kg calves within a 36-day interval was
not an intact pregnancy when fertilization occurred (Knaus, observed (Rao, Rao & Sivaiah, 1987). However, these
1967). For this condition Kussmaul (1859) developed the studies and many others have not been able to rule out
term ‘‘Superfetatio impropria’’. delayed implantation as a possible explanation (Harman,
1917; Nottle, 1976).
(6) Split parturition In an extensive experimental study Carter (2002) attemped
to induce SF in cows. While the experimental induction of SF
In split parturition, offspring from the same litter are born via artificial ovulation and insemination failed, he did succeed
over an extended interval. This phenomenon was described with the transfer of seven-day-old embryos until the 16th day
by Sparrow (1977) for the rat, and for breeding pigs by of pregnancy. Evaluation of examples of SF requires precise,
Vandeplassche (1969). Since another mating could definitely timed experiments, with a detailed reproductive history of
be excluded, the most likely explanation in these cases was the animals in question, often difficult to achieve in species
delayed nidation of several fertilized oocytes. with long pregnancies.
(3) Laboratory species

IV. EVIDENCE FOR SUPERFETATION
IN MAMMALS SF can be induced in rats and mice experimentally by
local injection of progesterone (Slonaker, 1934; Littleford &
Gysin, 1944; Canivenc & Mayer, 1955; Yoshinaga, 1961;
(1) Reproductive modes in mammals
Nakagawa, Yoshinaga & Hosi, 1966). Amazingly, when a
The Monotremata, Marsupialia and Eutheria all have rat is stimulated to carry two cohorts of fetuses at different
characteristic adaptations to achieve transfer of energy stages of development, it will time birth according to the
from mother to young first via the uterus and placenta, relative investment in each cohort. If the number of young
in the older cohort is greater than that in the younger musk rat (Ondatra zibetica; Stieve, 1952; Stieve-Miegel, 1955),
cohort then birth will occur at a time appropriate to the panther (taxonomic name not given; Anghi, Lehoczky &
older cohort with the younger cohort dying (Yoshinaga, Orbanyi, 1978) and sea lion (Zalophus californianus; Wandrey,
1971). 1977). Shorter interbirth intervals than the suspected
Inductions of SF have been attempted successfully pregnancy length have been reported for the Patas monkey
(Edwards & Fowler, 1958) and unsuccessfully (Bloch, 1952) (Erythrocebus patas; Leakey, 1969), lion (Panthera leo; Dathe,
in mice, with the successful cohorts spaced 2.5–3 days 1961), Geoffroy’s cat (Leopardus geoffroyi; Bartikova, 1978),
apart. Stowell (1941) described a case of possible SF in a and white-tailed deer (Odocoileus virginianus; Bartmann, 1971)
mouse with 15 days between successive litters. However, although this latter case may result from embryonic diapause.
it is unknown whether delayed implantation was involved, Gitlin & Adler (1968) describe a severe pathology in a
or whether a pre-partum copulation took place. Crew & chinchilla (Chinchilla laniger) where parallel intrauterine and
Mirskaia (1930) observed matings during pregnancy in mice, abdominal pregnancies at different developmental stages
confirmed by detection of vaginal plugs after insemination were discovered. Although this represents SF by definition,
(Rollhäuser, 1949). this is obviously a reproductive abnormality.
Other studies have also reported SF in mice and rats Stieve-Miegel (1955) found a suspected case of SF in
(Littleford & Gysin, 1944; Rollhäuser, 1949). Sparrow (1977) the musk rat where the first pregnancy was unilateral and
described the protracted delivery of one his laboratory a second set of ova had implanted during pregnancy in
rats which died after giving birth to six out of seven full- the contralateral uterine horn. Differences in the quality of
term infants. The seventh fetus remained in the uterus the CLs were identified histologically. Similar findings were
together with another six mid-term conceptuses growing in described for the European beaver (Castor fiber; Zurowski &
the opposing uterine horn. This is extraordinary considering Doboszynska, 1975). It appears therefore that while SF may
that litter size in rats is 4.6. Sparrow (1977) subsequently occur occasionally in these species (as in the mouse and rat),
estimated the incidence of SF in this particular colony to be it is not a consistent reproductive strategy; as these cases were
9–27 pregnancies in every 10,000. SF was suggested to be a rare and the offspring aborted.
heritable characteristic in mice but this was never confirmed Occasional cases of SF have also been suspected for several
(Leonard & Linden, 1972). Maceration and resorption of bat species (Table 1). De Bonilla & Rasweiller (1974), using a
fetuses is known to occur in the rat (Corey, 1933). Ibsen laboratory colony of Carrolia spp., observed ovulation during
(1928) found little or no evidence of SF or superfecundation pregnancy, fertilized ova in the oviduct during pregnancy,
in guinea pigs, but fetal resorption seemed to be fairly and CLs of different qualitiy, although they did not discuss
common. SF. In an Indian fruit bat, the Leschenault’s rousette (Rousettus
The European rabbit (Oryctolagus cuniculus) in its leschenaulti), different-sized fetuses were found in the uterus
domesticated form is often used as an experimental animal. (Karim & Gupta, 1986). As this species is monotocous with
This species is interesting to consider because of its relatively a bicornuate uterus and females only give birth to a single
close relationship to the European brown hare, in which SF young in each of two consecutive pregnancies each year,
is discussed to be a reproductive strategy (see Section V.3),
the discovery of a female with discordantly sized fetuses in
although current estimates suggest that they last shared a
both uterine horns and separate active CLs in both ovaries
common ancestor approximately 50 million years ago (Rose
fulfils the criteria for SF (Gopalakrishna & Choudhary,
et al., 2008). Pickard (1928) observed mating eight days before
1977).
birth with a second litter born 23 days after the first. Both
To date, there are three eutherian species reported to
litters were healthy and alive. Mayer & Klein (1946) induced
exhibit SF as a basic reproductive strategy (see Section V):
mating via administration of oestrogens in pregnant females
the American mink (Hansson, 1947; Shackelford, 1952), the
12 days after copulation. Dissection nine days later showed
European badger (Yamaguchi, Dugdale & Macdonald, 2006)
implanted fetuses but the earlier fetuses were dead and in a
and the European brown hare (Hediger, 1948). The mink
state of resorption. Stieve (1952) reported that a female rabbit
and the badger combine SF with delayed implantation and
gave birth to two litters within a 14-day interval, concluding
that SF must occur in rabbits. Bloch (1952) attempted to the offspring are all born on the same day; the hare probably
induce SF in rabbits but did not succeed. Taken together has a pre-partum oestrus with implantation occurring after
there is little evidence that SF might be a reproductive parturition (Bloch et al., 1967; Martinet, Legouis & Moret,
strategy in the rabbit. 1970). The swamp wallaby (Wallabia bicolor; Calaby & Poole,
1971; Paplinska et al., 2006) is a marsupial that also exhibits
characteristics of SF. These species are discussed in detail in
(4) Wildlife Section V.
SF has been reported in many different species of wildlife Pre-partum oestrus was suspected for the casiragua
(Table 1). Observations range from rare single cases to (Proechimys guairae; Weir, 1973) and the common gundi
the description of SF as a basic reproductive mechanism. (Ctenodactyles gundi; Gouat, 1985). In casiragua, 50% of
Observations of suspected rare cases of SF derive mainly from animals underwent a pre-partum oestrus 24–48 h before
animals in captivity. Cases in which fetuses of diffent size were parturition (Weir, 1974). However, no information was given
found inside the uterus or born at the same time include the concerning copulation, fertilization or subsequent pregnancy
in this species. In the American mink ovulation does not V. TRUE SUPERFETATION IN MAMMALS
occur until 48 h after copulation (Enders, 1952). Therefore,
it is possible that fertilization resulting from the pre-partum (1) The American mink
oestrus and copulation could occur after parturition in the
casiragua. This may also apply to the common gundi, in The reproduction of the American mink (Neovison (Mustela)
vison, Schreber 1777) has been extensively studied and
which a copulatory plug is present before parturition (Gouat,
described given that it has been bred for its valuable fur
1985).
since the beginning of the 20th Century (Hansson, 1947;
Enders, 1952; Lariviere, 1999). It gives birth to only one litter
per season. Mating takes place from February to April and
(5) Humans
parturition occurs in late June (Hansson, 1947; Sidorovich,
Extensive reviews and numerous case reports discuss the 1993). The onset of mating and gestation is controlled
possibility of SF in man (Kemkes, 1922; Sperling, 1926; by photoperiod (Duby & Travis, 1972; Hammond, 1951)
Neuhaus, 1954; Blickstein, 2003). Although extremely rare, but this can also be adjusted to external food resources
SF does seem to occur in humans. It is implied in cases as shown in certain areas of Alaska (Ben-David, 1997).
where the size difference in twins is approximately one Ovulation is induced by the presence of males or by
month, i.e. the length of another menstrual cycle (Fontana & attempted or successful copulation (Adams, 1981; Hansson,
Gilles, 1970; Scrimgeour & Baker, 1974; Baijal et al., 2007), 1947; Venge, 1959). Gestation length averages 51 days but
but as evaluation is not possible this remains a point of may vary from 40 to 75 days with females producing a
discussion. Since the advent of high-resolution ultrasound litter of four altricial young (range 2–8) (Hansson, 1947;
the visual detection of very early pregnancy has become Enders, 1952; Sidorovich, 1993). Dukelow (1966) showed
possible in humans. This sensitivity allows the detection that gestation length is dependent on litter size as well as
of early discordance during development of the human on the date of mating with later mating dates leading to
fetus. Tuppen et al. (1999) reported a case of probable SF shorter gestation length. Varying pregnancy length is caused
showing consistent developmental discordance and equal by delayed implantation or embryonic diapause which
growth velocities during the course of a twin pregnancy has been suggested to increase the female’s reproductive
over consecutive examinations. However, the possibility of fitness (Yamaguchi et al., 2004). The mink also exhibits
SF was strengthened after birth when inherited metabolic superfecundation which is achieved by multiple matings
and chromosomal abnormalities could be excluded. It still over a prolonged window of oestrus. Superfecundation
remains speculative whether a second ovulation took place. provides a mechanism whereby a female can avoid devoting
her entire reproductive effort to one male. However, the
Without evidence of multiple ovulations and their respective
chance of securing multiple fathers in one ovulation event is
CLs as well as the use of early ultrasonography fetal size
restricted to 1–3 days following the first mating (Johansson &
differences cannot always be attributed to SF (Rosenberg,
Venge, 1951). Thus, the female’s window of opportunity for
1954; Scrimgeour & Baker, 1974; Baijal et al., 2007).
polyandry is greatly extended by superfetation. Experiments
However, there is good evidence for SF in humans resulting
with matings at different time intervals showed that new
from the use of artificial reproductive technologies (Bonnar,
ovulations do not occur until seven days after the first
1865; Walter, Hasenohr & Kerin, 1975; Soudre et al., (Johansson & Venge, 1951). In the second ovulation cycle
1992; Dmowsky, De Orio & Rana, 1997; Steck & Bussen, additional ova are fertilized when the previous fertilized ova
1997). Harrison et al. (2005) demonstrated discordance in are already at the blastocyst stage in the uterus. Nevertheless,
development after the transfer of three embryos. After birth it is impossible to tell whether the pups in a litter arose from an
of three fetuses with growth discordance it was demonstrated early or late mating or from two or more matings (Johansson
by the method of ultrasound scanning of the developing & Venge, 1951). The uniformity in size and development of
gyri and sulci of the fetuses in question that there must the pups is an indication that implantation and development
have been two implantations from the embryo transfer began at approximately the same time (Enders, 1952). The
and another spontaneous fertilization and implantation use of fathers with different phenotypes to prove paternity
after another three weeks. Ultrasound examination is very indicated that with SF only 15% of the offspring were derived
reliable for determining gestational age (Slagle, Oliphant & from the first mating (Enders, 1952). Superfecundation was
Gross, 1989). Harrison et al. (2005) suggest that ultrasound demonstrated using a similar technique. More young survive
scanning and morphological evidence during the first from the first mating with increasing length of the mating
trimester are required for a definite diagnosis of SF. interval (Enders, 1952).
Other cases of idiopathic SF in humans appear to have To summarize the above, the American mink has a
been caused by endogenous reproductive complications second ovulation more than seven days after the first
such as the presence of ectopic pregnancy (Hartel, 1958; which results in two litters from different ovulation cycles
Honore & Nickerson, 1977; Van Dam, Vanderheyden & and different developmental stages present in the uterus,
Uyttenbroeck, 1988; Kobayashi et al., 1996) and in a case conforming to the classic definition of SF (Kussmaul,
of bicornuate uterus (Singhal et al., 2003), a rare uterine 1859). Yamaguchi et al. (2004) proposed that while delayed
abnormality. implantation enhances polyandry by superfecundation, the
window of mating is prolonged by SF in this species. Delayed paternities within social groups. As in the American mink the
implantation prevents discordance in development with all combination of reproductive strategies in the badger clearly
the offspring born together at the same developmental disguises paternity.
stage. This combination of diapause, superfecundation and
superfetation results in the potential of several fathers to one
litter and maximizes the potential number of implantations. (3) The European brown hare
However, in captive populations it has been shown that only SF has been assumed to exist in the European brown
84% of the eggs released are implanted and only 50% result hare (Lepus europaeus, Pallas 1778) at least since Aristotle
in young while the rest are resorbed (Hansson, 1947). This (Goold, 1979), and presumably developed from the fact that
mechanism of embryonic resorption may ‘‘sort’’ the fertilized offspring at different developmental stages were found inside
ova for quality but the underlying mechanisms are not well the uterus by hunters (Diezel, 1903) and by researchers
understood. Some of the many immunological factors acting (Stieve, 1952; Lienhardt, 1940; Raczynski, 1964). After
during pregnancy might play a role (Mor, 2006; Clark, 2008). Hediger (1948) established guidelines for successful captive
In free-ranging mink the male’s inability to monopolize breeding of brown hares, interbirth intervals shorter than
paternity is thought to be responsible for their lack of the mean pregnancy length of 42 days were consistently
territoriality (Yamaguchi et al., 2004). It is known that observed (Hediger, 1948; Martinet et al., 1970; Bürger,
polyandry can enhance fitness benefits for females (Jennions 1973; Sackmann, 1977; Slamečka & Šebová, 1991; Tocchini
& Petrie, 2000; Fisher et al., 2006; Klemme, Ylönen & et al., 2000). In large breeding colonies, mean interbirth
Eccard, 2008). The potential underlying mechanisms are intervals were 38–39 days (Martinet, Legouis & Moret,
complex including sperm competition and cryptic female 1970; Tocchini et al., 2000; Slamečka & Šebová, 1991).
choice (Jennions & Petrie, 2000). In males, paternity success, Other studies have reported values as low as 34 days
in terms of numbers of offspring fathered, does not equal (Bürger, 1973) or 24–27 days (Slamečka & Šebová, 1991).
fertilization success, in terms of oocytes fertilized, with the The incidence of shortened interbirth intervals in captive
difference due to paternal genetic effects influencing embryo populations appears variable with estimates of 66% (Martinet
viability (Garcia-Gonzalez, 2008). et al., 1970; Slamečka & Šebová, 1991) and 39.2% (Tocchini
et al., 2000). Slamečka & Šebová (1991) described successive
(2) The European badger increases in the incidence of shortened interbirth intervals
The biology of reproduction of the European badger over multiple years so that six litters per individual per year
(Meles meles; Linnaeus 1758) was extensively reviewed by were possible.
Yamaguchi et al. (2006). Like the American mink, it uses The mating of pregnant females, required for SF to
a combination of several reproductive tactics including exist, has been discussed in the literature for a long time
diapause and SF to enhance reproductive success. The (Diezel, 1903). Hediger (1948) was the first to observe
European badger has an optimum breeding season between mating of late-pregnant does with fertile males 2–3 days
late winter and early autumn and a gestation period of prior to parturition. He concluded that the mating of a
7–8 weeks giving birth to 1–6 young. This species also highly pregnant female 1–5 days before parturition was a
has embryonic diapause which can last up to 11 months regular event during the main breeding season; this was also
(Canivenc & Bonnin, 1981). Thus, females mate and are noted by others (Bloch et al., 1961; Caillol & Martinet, 1976,
usually pregnant with multiple embryos in diapause by 1983). Nevertheless, it was not clear if this mating coincided
early summer. It is suggested that due to the loss of with ovulation. Behavioural evidence for the existence of
embryos in diapause, females continue to ovulate during a pre-partum oestrus in the brown hare has been reported
the non-breeding season in order to maintain the supply (Stieve, 1952; Bloch et al., 1961). Increased mating behaviour
of dormant embryos prior to reactivation (Yamaguchi et al., of females was observed from day 34 of gestation until
2006). Evidence to support this includes multiple peaks of parturition (day 38 on average) (Caillol & Martinet, 1981,
oestradiol between late spring and early autumn (Mondain- 1983; Martinet, 1980). This mating before birth was not
Monval et al., 1980), an increase in the number of CLs during inhibited by elevated serum progesterone levels during late
diapause without any associated increase in the number of pregnancy (Martinet, 1980; Caillol & Martinet, 1981). It has
blastocysts (Creswell et al., 1992; Page, Ross & Langton, been shown subsequently that follicular development and
1994), and the presence of immature blastocysts during late growth can occur throughout pregnancy, and this increases
diapause (Creswell et al., 1992). This last point is noteworthy just before birth (Martinet, 1980). CLs of different size and
because the size of blastocysts in diapause has been shown therefore age have been found during dissections in late-
to increase linearly with time due to fluid accumulation and pregnant females by several authors (Raczynski, 1964; Bloch
gradual growth of the trophoblast such that embryos that et al., 1967; Flux, 1967). The artificial induction of ovulation
have spent more time in diapause are larger than those in pregnant females using human chorionic gonadotropin
resulting from more recent fertilization (Creswell et al., 1992; succeeded between day 14 and 28 post conception but
Renfree & Shaw, 2000). Recently Dugdale et al. (2007) found caused abortion (Martinet, 1980). Luteinizing-hormone-
evidence in the European badger for multiple paternities in releasing-homone application in pregnant females induced
litters of free-ranging populations and also for extra-group ovulation throughout pregnancy (Caillol et al., 1991a). Thus,
both the ovary and pituitary are sensitive to induction of breeding would be more frequent because the female cannot
ovulation. By contrast, natural ovulation induction by mating take flight from the male.
only succeeded after day 34 of pregnancy. Therefore, it Even though SF in the European brown hare has been
was concluded that Graafian follicles developed prior to suspected for centuries to be a regular event, the above
parturition and may be responsible for oestrus activity and discussion makes clear that the exact mechanisms that govern
mating (Caillol et al., 1991a). Increased mating behaviour reproduction in the hare are far from understood. The
may be required to stimulate the pituitary-hypothalamic- optimum time for induction of SF in this species appears to
gonadal axis to overcome the inhibition caused by an active be a short period of days before parturition, in contrast to
pregnancy (Caillol, Mondain-Monval & Rossano, 1991b). cases of SF in other mammals, such as humans, American
The precise mechanism by which ovulation occurs during mink or European badger, where SF mainly occurs at an
pregnancy is still unknown (Caillol et al., 1991a). early stage of pregnancy. By definition, SF requires ova
Morulae were found in oviductal flushings in two late- derived from different ovulation cycles. In most mammals,
pregnant females after death, providing evidence for pre- the length of the oestrus cycle is shorter than pregnancy
partum ovulation (Bloch et al., 1967; Martinet et al., 1970). length meaning that the second fertilization is likely to occur
It has not been established whether the passage of sperm near the beginning of the pregnancy. Also, this is the only
through the pregnant hare uterus is possible. The brown hare time period in species with a single uterus (such as humans),
has a bicornuate uterus with half of all pregnancies described where it is considered possible for sperm to pass through
as unilateral (Flux, 1967; Zörner, 1980). The uterine horn the pregnant uterus. Therefore, SF, in which the potential
ipsilateral to a pregnancy would be empty, so spermatozoa mating occurs a couple of days before birth is in contrast to
potentially could pass through it to fertilize newly released these other cases.
ova (Stieve, 1952; Watzka, 1959). However, it is not known Considering the evidence for SF in the European brown
how spermatozoa would reach the oviduct in the case of a hare it is of interest to consider whether a similarly complex
bilateral pregnancy. As an alternative it was suggested that reproductive strategy is present in other lagomorphs. The
semen could be stored from an earlier insemination with family Leporidae contains one large genus Lepus, generally
the mating before birth serving only to induce ovulation, known as hares, inhabiting all climatic regions and continents
and therefore SF. Martinet & Raynaud (1972) examined this (due to human introduction) except Antarctica, and a number
hypothesis and successfully mated one late-pregnant female of small genera of rabbits (Flux & Angermann, 1990).
with a vasectomised buck. After parturition, early embryonic There are remarkable differences in reproductive physiology
stages were flushed from the oviduct and they concluded that between hares and rabbits. While hares develop precocial
sperm storage had occurred for 30 days. Unfortunately, there young and therefore have a longer pregnancy (40–50 days),
was no description of the surgical technique. In a subsequent rabbits give birth to relatively altricial young and the length of
study they histologically examined the uterine glands in a pregnancy does not exceed 30 days (Niethammer & Krapp,
pregnant female and found semen up to day 17 of pregnancy 2003). Evidence for SF in the European rabbit was reviewed
(Martinet & Raynaud, 1973). However, since then no further in Section IV.3, where it was concluded that SF is not
evidence for this hypothesis has been presented. part of the reproductive strategy of this leporid lagomorph.
Stavy & Terkel (1992) tried to induce SF experimentally Lepus species are seasonally polyoestric and gonadal activity
using artificial insemination (AI) in late-pregnant females. is dependent on photoperiod. Depending on latitude and
While this was not successful, AI before birth (38 days) climatic factors only 1–2 litters are born per year in the
induced an earlier parturition. They subsequently inter- mountain hare L. timidus (Niethammer & Krapp, 2003) while
preted the previous findings of shortened interbirth intervals reproduction takes place all year round in the Cape hare
as a parturition mechanism, concluding that SF does not L. capensis mediterraneus (Niethammer & Krapp, 2003) and the
exist in this species. However, in contrast to other authors Indian hare L. nigricollis dayanu (Prakash & Taneja, 1969).
(see above) they reported no evidence for shortened inter- Little is known about the reproductive biology of most Lepus
birth intervals in their captive population, and speculated species. Only a few have bred in captivity to allow evaluation
that they may have bred a different species (L. capensis) in of reproductive parameters. The Japanese hare L. brachyurus
their colony. (Otsu, 1973; Takeda, Torii & Aiko, 1994) has a pregnancy
Some authors have discussed the existence of SF in the length of 43–45 days and is a second example within this
European brown hare giving the cessation of the function of genus for which shortened interbirth intervals (two cases, 33
the CL and the possibility of natural growth retardation of the and 34 days) have been observed (Takeda et al. 1994). SF has
fetuses as explanation for apparent SF (Knaus, 1966). Others been excluded in the jackrabbit L. californicus (Lechleitner,
concluded that SF was a result of captive breeding (Rieck, 1959) and the Iberian hare L. granatensis (Alves et al., 2002)
1956; Raczynski, 1964) and was irrelevant to free-ranging although it is unclear what criteria were used to determine
populations (Broekhuizen & Maaskamp, 1981). However, in this. The Alaskan hare L. othus and the Arctic hare L. arcticus
studies in New Zealand (Flux, 1967), SF was calculated to usually only deliver one litter per year (Anderson & Lent,
occur naturally in 13% of pregnancies based on observations 1977) probably making SF redundant in these species. The
of differing CLs in three out of 24 pregnancies with fully existence of SF in other Lepus species remains a topic for
developed fetuses. It was predicted that SF in captive future research.
The second taxonomic family in the order Lagomorpha, milk per day, while the opposing lactating gland may pro-
the pikas (Ochotonidae), give birth to altricial young similar duce 40–50 ml per day of a high-fat, high-protein, low-sugar
to those of rabbits and there is currently no evidence for SF milk suitable for a young at late pouch life or early indepen-
in this group (Nowak, 1991). dence (200–300 days post-partum; Green & Renfree, 1982;
Green & Merchant, 1988; Green, Merchant & Newgrain,
(4) Macropodid marsupials 1988). There are also changes in the expression of specific
milk proteins that are switched on and off during the different
The swamp wallaby (Wallabia bicolor), like other macropodid phases of lactation in this species (Nicholas, 1988). To date,
marsupials, has two anatomically separate uteri and also this process still remains a physiological mystery. However,
three vaginas, of which the two lateral vaginas swell with given that marsupials exit the pouch at an equivalent devel-
semen upon mating providing passage for sperm to the opmental stage to that at which many precocial eutherian
uteri while the median vagina only becomes patent at birth species are born, ‘‘exchanging the umbilical cord for the
allowing delivery of the young (Tyndale-Biscoe & Renfree, teat’’ (Renfree, 1983; Renfree, 2009, p.1), there are obvious
1987). While this reproductive anatomy would apparently parallels between the local control required for concurrent
lend itself to SF, the majority of kangaroos and wallabies asynchronous lactation in marsupials and superfetation. In
rely on this design to implement their highly successful this context, parturition represents an arbitrary time-point in
reproductive strategy involving embryonic diapause. All the development of mammals. In combination with embry-
macropodid marsupials, except the western grey kangaroo onic diapause, it is believed that concurrent asynchronous
(Macropus fuliginosis; Tyndale-Biscoe & Renfree, 1987), are lactation is part of a wider strategy in macropodid marsupials
capable of mating during their extensive lactation period. to maximize the output of young in an uncertain climatic
However, upon reaching the blastocyst stage, the new environment. This may also be one of the reasons for the
conceptus becomes metabolically quiescent; its development evolution of SF in poeciilid fish discussed below (Sadlier,
is not reactivated until seasonal or lactational inhibition 1965; Newsome, 1965). Given this suggestion, it may be
ceases (Tyndale-Biscoe & Renfree, 1987). The swamp that mammals displaying superfetation are simply ensuring
wallaby is the only macropodid marsupial known to date against loss of their first litter.
to have an oestrous cycle shorter than its gestation length
(31.0 and 35.5 days, respectively; Paplinska et al., 2006). Thus
the swamp wallaby is likely to mate pre-partum, after which
the new embryo enters diapause. This system would meet the VI. SUPERFETATION IN NON-MAMMALIAN
definition of SF as there are two asynchronous conceptuses VERTEBRATES
that develop simultaneously from separate oestrous cycles.
Swamp wallabies are solitary animals that live a nomadic Examples of viviparity exist in all vertebrate groups except
lifestyle and are responsive to human disturbance. SF may birds (Rothchild, 2003). This character is particularly preva-
have evolved in this animal to extend the period of receptivity lent in fish, having evolved independently on many occasions.
and ensure that the chance encounter of a male occurs prior SF has been described in numerous species of fish within the
to birth (35 days), and the subsequent onset of lactational families Poeciliidae and Zenarchopteridae which also sup-
reproductive quiescence. However, definitive evidence of SF port varying degrees of maternal provisioning and basic
will only come from the simultaneous observation of a late- placentation (Soong, 1968; Roberts, 1989; Meisner & Burns,
stage fetus and an early-stage conceptus within this animal. 1997; Reznick, Mateos & Springer, 2002; Reznick, Meredith
While swamp wallabies breed continuously in captivity, they & Collette, 2007) (Table 2). As stated by Reznick et al. (2007)
are very susceptible to capture myopathy and stress, and concerning placentation, the study of SF in fish can tell us
intensive monitoring and capture to better describe this much about the selection forces driving this process because
phenomenon has thus far failed, presumably due to stress- it has evolved many times and is highly variable compared
related effects during pregnancy. to the mammalian model in which characters like viviparity
Continuously breeding macropodid marsupials (kanga- and placentation presumably evolved once in a common
roos and wallabies) such as the red kangaroo (Macropus ancestor some 150 million years ago (Bininda-Emonds et al.,
rufus) and agile wallaby (Macropus agilis) are also capable 2007). Reznick & Miles (1989) suggest that SF evolved inde-
of ‘‘concurrent asynchronous lactation’’ whereby a female pendently at least four times within the family Poeciliidae.
can support the nutritional requirements of two different The ability to ‘‘gestate’’ embryos within either the ovarian
young at different developmental ages (Sharman & Calaby, follicles or within the ovarian lumen is unique to live-
1964; Sharman & Pilton, 1964; Lemon & Barker, 1967; bearing fish. Meisner & Burns (1997) suggest that the
Griffiths, McIntosh & Leckie, 1972; Lincoln & Renfree, intra-follicular condition may represent an intermediate
1981). During concurrent asynchronous lactation, adja- stage between lecithotrophic species (those in which the
cent mammary glands can produce milk of very different embryos rely solely on nutrients supplied from the egg)
composition and quantity (Green, Newgrain & Merchant, and matrotrophic species (those in which there is some
1980). Under experimental conditions in the tammar wallaby degree of maternal provisioning to the developing embryo in
(Macropus eugenii), an early-stage young (0–30 days post- addition to the egg). While some species with intra-follicular
partum) may consume up to 1 ml of a dilute, high-sugar development display matrotrophy, all teleost species with
Table 2. Fish species exhibiting superfetation (SF) and other characteristics of maternal care. Y, yes; LB, live bearing; PNC,
post-natal care; MP, maternal provisioning
Order SF Other features of maternal care Reference

Family
Taxonomic name
Beloniformes
Zenarchopteridae
Dermogenys bispina Y LB, PNC Meisner (2001)
Dermogenys orientalis Y LB, PNC Meisner (2001)
Dermogenys pusilla Y LB, PNC Meisner (2001)
Dermogenys sumatrana Y LB, PNC Meisner (2001)
Dermogenys robertsi Y LB, PNC Meisner (2001)
Dermogenys bruneiensis ? LB Meisner (2001)
Dermogenys palawanensis ? LB Meisner (2001)
Nomoramphus liemi ? LB Meisner (2001)
Nomoramphus celebensis ? LB Meisner (2001)
Nomoramphus ebrardtii ? LB, PNC Meisner (2001)
Nomoramphus pinnamaculata ? LB, PNC Meisner (2001)
Nomoramphus brembachi Y LB, PNC Meisner (2001)
Nomoramphus pectoralis Y LB, PNC Meisner (2001)
Nomoramphus manifesta Y LB, PNC Meisner (2001)
Nomoramphus rossi Y LB, PNC Meisner (2001)
Cyprinodontiformes
Poeciliidae
Poeciliopsis turrubarensis Y LB, varying MP Zúñiga-Vega et al. (2007)
Poeciliopsis monacha Y LB Thibault & Schultz (1978)
Poeciliopsis lucida Y LB, MP Thibault & Schultz (1978)
Poeciliopsis prolifica Y LB, MP Thibault & Schultz (1978)
Poeciliopsis turneri Y LB, extensive MP Thibault & Schultz (1978)
Poeciliopsis occidentalis Y Scrimshaw (1944)
Poecilistes pleurospilus Y Scrimshaw (1944)
Pseudopoecilia fria Y Scrimshaw (1944)
Diphyacantha chacoensis Y Scrimshaw (1944)
Priapella bonita Y Scrimshaw (1944)
Phalloptychus januarius Y Scrimshaw (1944)
Micropoecilia branneri Y Scrimshaw (1944)
Heterandria formosa Y LB, MP Turner (1937)
intra-luminal ovarian development are thought to display It is not clear why SF has evolved in some fish species
matrotrophy. rather than others. Perhaps it facilitates greater genetic
In fish species exhibiting SF (Table 2), cohorts of embryos diversity by ensuring that different broods are fertilized by
(normally one to four) traverse the ovaries from the ante- different fathers. However, it is unknown whether subsequent
rior to posterior ends, with individual cohorts spaced at fertilizations occur from stored sperm or whether they result
varying intervals depending on the species. The phe- from separate matings (Reznick et al., 2002).
nomenon is most pronounced in Heterandria spp. where Recently, Zúñiga-Vega, Reznick & Johnson (2007)
up to eight broods can develop at the same time and demonstrated that habitat type may explain the evolution of,
are spaced approximately 2–3 days apart (Turner, 1937).
and variability in, SF forms seen in Poeciliopsis turrubarensis.
Given that SF has also evolved in species that lack maternal
They predicted that staggering cohorts of embryos using
provisioning (matrotrophy), the process was possibly facil-
itated by embryo development being largely autonomous SF may be an evolutionary mechanism for maintaining
(Trexler & De Angelis, 2003). Therefore, coordination a streamlined body morphology within variable stream
of the maternal endocrine or provisioning systems with habitats and found marked variation in number, qual-
individual cohorts may not be required. Indeed, it is not ity, and spacing of embryo cohorts depending on stream
known in fish whether different cohorts at different stages velocity and body shape. Thus, simlar to the staggered
of development require variable physiological conditions reproductive strategy of macropodid marsupials, SF may
from the mother, as would be required during mammalian have evolved in fish in response to variable environmental
pregnancy. conditions.
VII. DISCUSSION pregnancy. In mammals pregnancy is considered to be viable

young within the reproductive tract. Normally, it is associated
In the European brown hare, five centuries of speculation and with implantation into the uterus and placentation. Stölting
many scientific studies over the past 80 years have provided & Wilson (2007), in connection with the reproduction of
some evidence for SF, but the underlying mechanisms are seahorses, discussed whether the term pregnancy might
not understood. The most probable explanation of the data be especially reserved for mammals. Many vertebrates
is that conception occurs shortly prior to parturition, but this support basic placentation, e.g. live-bearing fish, yet they
would be unique among mammals. If SF occurs in every do not have a specialized compartment like the mammalian
pregnancy, fertilization 3–5 days before birth would mean uterus. Birds have a uterus that harbours young during
a maximum gain of approximately half a pregnancy length the earliest embryonic stages while the egg is forming, but
over a whole breeding season implying there is unlikely to there is no further maternal provisioning to the embryo
be a significant reproductive benefit from SF in this species. in addition to that supplied within the egg. Thus the
However, hares are reported to live up to 6 or 7 years in term pregnancy can be linked to a stage of maternal
the wild with individuals as old as 12 years being reported provisioning to the conceptus within the mother. One
(Pielowski, 1971) so the accumulated occurrence of SF over could argue then that this does not extend to mammalian
many breeding seasons may be reproductively beneficial. pre-implantation stages. However, after fertilization, the
The reproductive biology of other leporids is very poorly mammalian embryo does receive micronutrients to sustain
characterised, especially with regards to the presence of SF. vital functions for continued development, and in the case
In the European badger and the American mink, SF of embryonic diapause, potentially a development inhibition
occurs in combination with other reproductive phenomena signal. Do these constitute maternal provisioning for normal
including embryonic diapause. development? Until these ambiguities are resolved whether
So why is SF found in these three species and not in species such as the badger can be defined as exhibiting SF
others? Although the European brown hare population will remain unclear.
is thought to be declining and it is even endangered in At present the term ‘‘superfetation’’ is used for several
some European countries (Pielowski, 1990; Hansen, 1992; conditions in reproductive biology which need to be more
Schäfers, 1996; Hell, Flak & Slamečka, 1997; Haerer et al., clearly defined and possibly renamed. Based on this review
2001), it is an evolutionary success story, inhabiting nearly we can now define several different functional categories of
all continents of the world. After its introduction to Australia this phenomenon (Fig. 1). We have divided SF into two main
and Argentina it spread rapidly colonising new habitats categories: accidental SF due to anatomical disorders (e.g.
and creating considerable problems for native wildlife and in humans, Singhal et al., 2003) or severe pathologies (e.g.
agriculture (Myers, Parer & Richardson, 1989; Bonino & abdominal pregnancies in the chinchilla; Gitlin & Adler,
Montenegro, 1997). The same is true for the American mink 1968), and true SF comprising ovulation and fertilization
during an intact active pregnancy. True SF can then be
which has now colonised many parts of Europe (Mitchell-
separated into artificial SF, due to the use of artificial
Jones et al., 1999). Recent cytogenetic and biochemical data
reproductive technologies (e.g. in cattle, Carter, 2002), and
support placement of the American mink in the genus Neovison
natural SF. The natural cases can again be divided into two
rather than in Mustela (Wozencraft, 2005) distancing it from
categories: ‘Extremely rare’ describes cases where SF is very
the European mink (Mustela lutreola). The European mink
rare and not considered part of normal reproductive biology
is cited by Mitchell-Jones et al. (1999) as an endangered
(e.g. in humans). To date, this includes all the SF cases
species and its decline in some areas has been attributed to
where fetuses of different size were found in the uterus of a
land-use practices leading to a loss of suitable habitat. In
pregnant female and we propose calling this ‘superfetation
central Europe its population was formerly severely reduced
proper’. The ‘regular’ category unites the known eutherian
by rabies, but that threat has now decreased with rabies
species exhibiting SF as reproductive strategy. SF combined
controls (Mitchell-Jones et al., 1999). Whether competition
with diapause as in the American mink and European badger
with American mink has contributed to its decline is
comprises a group with a pre-implantation oestrus and should
controversial (Youngman, 1990). Many mustelids exhibit
be reclassified as ‘‘superfertilization’’. SF as seen in the
an implantation delay (34% of Mustelidae show embryonic
European brown hare with a pre-partum oestrus but probably
diapause) (Lindenfors, Dalen & Angerbjörn, 2003; Thom,
with implantation after parturition should be reclassified as
Johnson & Macdonald, 2004). However, data from levels of
‘‘superconception’’. This scheme (Fig. 1) will hopefully allow
faecal progestagens and CL development in European mink
more accurate description of future observations of SF in
strongly suggest that there is no implantation delay in this
mammals.
species, as has also been shown for the European polecat
(Mustela putorius) (Amstislavsky et al., 2009). Therefore, the
American mink and the European mink seem to have evolved
very different reproductive mechanisms possibly giving the VIII. CONCLUSIONS
invasive American mink a reproductive advantage.
SF is defined as ovulation and conception during an (1) Superfetation (SF) is the process of ovulation and
intact pregnancy. This requires an accurate definition of fertilization during an intact pregnancy and the
SUPERFETATION (SF)
TRUE SF: ACCIDENTAL SF:

Intact pregnancies, no SF in connection with
negative impact on mother severe pathologies
TRUE ARTIFICIAL SF
TRUE NATURAL SF via artificial reproductive technologies
Regular: Extremely rare:

suspected part of reproductive physiology not part of reproductive physiology
Shortened interbirth Fetuses of different size; offspring

intervals, new conception are born with age difference
prior to parturition equivalent to cycle length (or to a
multiple of cycle length)
SF combined with
embryonic Diapause
pre-partum pre-implantaion
oestrus oestrus
Superconception Superfertilization Superfetation proper

e.g. European e.g. American mink, e.g. Humans
brown hare European badger
A
(F = fertilization; I = implantation; P = parturition)

1. Pregnancy
F I P
Superconception F I P
2. Pregnancy
Superfetation proper F I P
Superfertilization F I P B
Fig. 1. (A) Classification scheme to separate cases of reported superfetation (SF) in mammals. (B) Schematic explanation of the
different modes of SF.
development of two litters at different developmental (2) Reviewing the current literature it is clear that
stages. However, evidence for SF may be confused SF may occur in several species but is usually a
with the resumption of ovarian cyclicity resulting from rare reproductive abnormality. There is no mammal
an aborted pregnancy or during a period of embryonic species for which SF proper (i.e. the finding of
diapause which may not technically be defined as an fetuses of different developmental stages inside the
active pregnancy. In no reported cases of SF have uterus, Fig. 1), has been adequately demonstrated to
these criteria been tested fully. Unusual reproductive be an evolved reproductive strategy.
observations in any species can only be evaluated (3) A new classification scheme is developed to separate
where exact data are available. cases of SF in mammals.
(4) The reproductive mechanisms that allow ovulation, Caillol, M. & Martinet, L. (1976). Preliminary results on plasma progesterone
levels during pregnancy and superfetation in the hare, Lepus europaeus. Journal of
fertilization and development of a new conceptus prior Reproduction & Fertility 46, 61–64.
to the delivery of an existing pregnancy clearly require Caillol, M. & Martinet, L. (1981). Estrous behaviour, follicular growth and pattern
further investigation. of circulating sex steroids during pregnancy and pseudopregnancy in the captive
brown hare. In Proceedings of the World Lagomorph Conference (eds. K. Meyers and
C. D. MacInnes), pp. 142–154. University of Guelph, Guelph & IUCN.
Caillol, M. & Martinet, L. (1983). Mating periods and fertility in the doe hare
(Lepus europaeus) bred in captivity. Acta zoologica fennica 174, 65–68.
Caillol, M., Mondain-Monval, M., Meunier, M. & Rossano, B. (1991a).
IX. ACKNOWLEDGEMENTS Pituitary and ovarian responses to luteinizing-hormone-releasing hormone (LHRH)
during pregnancy and after parturition in brown hares (Lepus europaeus). Journal of
Reproduction & Fertility 92, 89–97.
We thank our librarians Cornelia Greulich and Beate Peters- Caillol, M., Mondain-Monval, M. & Rossano, B. (1991b). Gonadotrophins and
Mergner, Barbara Drews for her constructive criticism and sex steroids during pregnancy and natural superfetation in captive brown hares
Heribert Hofer and others who helped with professional (Lepus europaeus). Journal of Reproduction & Fertility 92, 299–306.
Calaby, J. H. & Poole, W. E. (1971). Keeping kangaroos in captivity. International
discussions on this topic. Zoo Yearbook 11, 5–12.
Canivenc, R. & Bonnin, M. (1981). Environmental control of delayed implantation
in the European badger (Meles meles). Journal of Reproduction & Fertility, Supplements 29,
25–33.
Canivenc, R. & Mayer, G. (1955). Contribution a l’etude experimentale de la
X. REFERENCES superfetation chez la rate. Recherches basees sur la nidation retardee. Annales
d’endocrinologie 16, 1–33.
Carter, J. A. (2002). Superfetation in Beef Cattle. Dissertation, Louisiana State University.
Adams, C. E. (1981). Observations on the induction of ovulation and expulsion of
Clark, D. A. (2008). Immunological factors in pregnancy wastage: fact or fiction.
uterine eggs in the mink, Mustela vison. Journal of Reproduction & Fertility 63, 241–248.
American Journal of Reproductive Immunology 59, 277–300.
Alves, P. C., Goncalves, H., Santos, M. & Rocha, A. (2002). Reproductive
Corey, E. L. (1933). The maceration and resorption of fetuses in the rat. The Anatomical
biology of the Iberian hare, Lepus granatensis, in Portugal. Mammalian Biology 67,
Record 56, 195–209.
358–371.
Creswell, W. J., Harris, S., Cheeseman, C. L. & Mallinson, P. J. (1992).
Amstislavsky, S., Lindeberg, H., Ternovskaya, Y., Zavjalov, E., Zudova, G.,
To breed or not to breed: an analysis of the social and density-dependent constraints
Klochkow, D., Gerlinskaya, L. (2009). Reproduction in the European mink
on the fecundity of female badgers (Meles meles). Philosophical Transactions of the Royal
Mustela lutreola: oestrus cyclicity and early pregnancy. Reproduction of Domestic Animals
Society of London B 338, 393–407.
44, 489–498.
Crew, F. A. E. & Mirskaia, L. (1930). Mating during pregnancy in the mouse. Nature
Anderson, H. L. & Lent, P. C. (1977). Reproduction and growth of the tundra hare
125, 564.
(Lepus othus). Journal of Mammalogy 58, 53–57.
Dalrymple, D. B. H. & Jenkins, D. (1951). A probable case of superfetation in the
Anghi, Cs. G., Lehoczky, Z. & Orbanyi, I. (1978). Superfoetation bei Panthern.
bovine. Cornell Veterinarian 41, 340–341.
Zoologischer Garten NF 48, 189–191.
Dathe, H. (1961). Superfoetation beim Löwen. Zoologischer Garten NF 25, 410–411.
Arbeiter, K. (1965). Zur Superfetation beim Pferd. Deutsche Tierärztliche Wochenschrift
De Bonilla, H. & Rasweiller, J. J. (1974). Breeding activity, preimplantation
72, 1–3.
development, and oviduct histology of the short-tailed fruit bat, Carollia, in captivity.
Baijal, N., Sahni, M., Neeraj, V., Kumar, A., Parkhe, N. & Puliyel, J. M. The Anatomical Record 179, 383–404.
(2007). Discordant twins with the smaller baby appropriate for gestational age Diezel, K. E. (1903). Niederjagd. Paul Parey, Berlin.
- unusual manifestation of superfoetation: A case report. BMC Pediatrics 7, 1–5. Dmowsky, W. P., De Orio, L. & Rana, N. (1997). Embryo implantation during
Baker, R. J., Makova, K. D. & Chesser, R. K. (1999). Microsatellites indicate a menstruation in the absence of adequate estradiol and progesterone support, with
high frequency of multiple paternity in Apodemus (Rodentia). Molecular Ecology 8, subsequent normal response to ovulation induction and superfetation. Fertility &
107–111. Sterility 68, 538–541.
Barnett, S. A. & Munro, K. M. H. (1970). Superfoetation of mice. Nature 227, Duby, R. T. & Travis, H. F. (1972). Photoperiodic control of fur growth and
1343–1344. reproduction in the mink (Mustela vison). Journal of Experimental Zoology 182, 217–226.
Bartikova, J. (1978). Superfoetation bei der Salzkatze Leopardus geoffroyi d’Orbigny Dugdale, H. L., Macdonald, D.W., Pope, L. C. & Burke, T. (2007). Polygy-
und Gervais 1844. Zoologischer Garten NF 45, 462–463. nandry, extra-group paternity and multiple-paternity litters in European badger
Bartmann, W. (1971). Superfetation beim Virginia-Hirsch (Odocoileus virginianus (Meles meles) social groups. Molecular Ecology 16, 5294–306.
Zimmermann 1780)? Zeitschrift für Säugetierkunde 36, 200–201. Dukelow, W. R. (1966). Variations in gestation length of mink (Mustela vison). Nature
Ben-David, M. (1997). Timing of reproduction in wild mink: the influence of spawning 211, 211.
Pacific salmon. Canadian Journal of Zoology 75, 376–382. East, M. L., Burke, T., Wilhelm, K., Greig, C. & Hofer, H. (2003). Sexual
Bininda-Emonds, O. R., Cardillo, M., Jones, K. E., MacPhee, R. D., Beck, conflicts in spotted hyenas: male and female tactics and their reproductive outcome
R. M., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L. & Purvis, A. with respect to age, social status and tenure. Proceedings of the Royal Society of London B
(2007). The delayed rise of present-day mammals. Nature 446, 507–12. 270, 1247–1254.
Blickstein, I. (2003). Superfecundation and superfetation: lessons from the past on Edwards, R. G. & Fowler, R. E. (1958). The experimental induction of
early human development. Journal of Maternal-Fetal & Neonatal Medicine 14, 217–219. superfetation in the mouse. Journal of Endocrinology 17, 223–236.
Bloch, S. (1952). Untersuchungen über Superfetation an der Maus. Schweizerische Egberts, J. & Fontyne, P. (1977). Superfoetation following artificial insemination in
Zeitschrift Medizinische Wochenschrift 24, 632–637. a ewe. Tijdschrift voor diergeneeskunde 15, 1312–1314.
Bloch, S., Hediger, H., Lloyd, H. G., Müller, C. & Strauss, S. (1967). Enders, R. K. (1952). Reproduction in the mink (Mustela vison). Proceedings of the American
Beobachtungen zur Superfetation beim Feldhasen (Lepus europaeus). Zeitschrift für Philosophical Society 96, 691–755.
Jagdwissenschaften 13, 49–52. Fisher, D. O., Double, M. C., Blomberg, S. P., Jennions, M. D. & Cockburn,
Bloch, S., Hediger, H., Müller, C. & Strauss, F. (1961). Probleme der A. (2006). Post-mating sexual selection increases lifetime fitness of polyandrous
Fortpflanzung des Feldhasen. Revue Suisse de Biologie 61, 485–490. females in the wild. Nature 444, 89–92.
Bonino, N. & Montenegro, A. (1997). Reproduction of the European hare in Flux, J. E. C. (1967). Reproduction and body weights of the hare Lepus europaeus in
Patagonia. Acta Theriologica 42, 47–54. New Zealand. New Zealand Journal of Science 10, 357–401.
Bonnar, G. L. (1865). A critical inquiry of superfetation, with cases. Edinburgh Flux, J. E. C. & Angermann R. (1990). Chapter 4: The Hares and Jackrabbits. In
Medicinal Journal 10, 2. Rabbits, Hares & Pikas: Status Survey & Conservation Action Plan (IUCN/ SSP Lagomorph
Broekhuizen, S. & Maaskamp, F. (1981). Annual production of young in European Specialist Group) (eds. J. A. Chapman & J. E. C. Flux), pp. 61–94. Gland, Schweiz.
hares (Lepus europaeus) in the Netherlands. Journal of Zoology 193, 499–516. Fontana, J. & Gilles, R. G. M. (1970). Superfetation. Obstetrics and Gynecology 35,
Bürger, M. (1973). Weitere Beobachtungen zur Zucht des Europäischen Feldhasen, 585–588.
Lepus europaeus Pallas, in Gefangenschaft. Zoologischer Garten NF 43, 275–277. Garcia-Gonzalez, F. (2008). Male genetic quality and the inequality between
Burton, C. (2002). Microsatellite analysis of multiple paternity and male reproductive paternity success and fertilization success: consequences for studies of sperm
success in the promiscuous snowshoe hare. Canadian Journal of Zoology 80, 1948–1956. competition and the evolution of polyandry. Evolution 62-7, 1653–1665.
Busch, W. & Waberski, D. (2007). Künstliche Besamung bei Haus- und Nutztieren. Geisert, R. D. (1998). Pigs—Embryonic mortality. In Encyclopedia of Reproduction,
Stuttgart: Schattauer. Vol. 3. (eds: E. Knobil and J. P. Neill), p. 798. Academic press, San Diego.
Gitlin, G. & Adler, J. H. (1968). Coexisting intrauterine and abdominal Husen, B., Adamski, J., Rune, G. M. & Einspanier, A. (2001). Mechanisms of
(intraperitoneal) pregnancy with possible superfoetation (superfecundation) and estradiol inactivation in primate endometrium. Molecular & Cellular Endocrinology 171,
with adhesion of placenta to foetus in a chinchilla (Chinchilla laniger). Acta Zoologica et 179–185.
Pathologica Antverpiensa 49, 65–76. Ibsen, H. L. (1928). Prenatal growth in guinea-pigs with special reference to
Goold, G. P. (ed) (1979). V Superfetation. In Aristotle XIII Generation of animals, p. 447. environmental factors affecting weight at birth. Journal of Experimental Zoology 51,
Loeb Classical Library. Cambridge, Massachusetts: Harvard University Press, 51–93.
London: William Heinemann. Jennions, M. D. & Petrie, M. (2000). Why do females mate multiply? A review of
Gopalakrishna, A. & Choudhary, P. N. (1977). Breeding habits and associated the genetic benefits. Biological Reviews 75, 21–64.
phenomena in some Indian bats, Part I - Rousettus leschenaulti (Desmarest) - Johansson, M., Bromfield, J. J., Jasper, M. J. & Robertson, S. A. (2004). Semen
Megachiroptera. Journal of Bombay National History Society India 74, 1–16. activates the female immune response during early pregnancy in mice. Immunology
Gopalkrishna, A. & Ramakrishna, P. A. (1977). Some reproductive anomalies in 112, 290–300.
the Indian rufus horse-shoe bat, Rhinolophus rouxi (Temminck). Current Science 46, Johansson, I. & Venge, O. (1951). Relation of the mating interval to the occurrence
767–770. of superfetation in the mink. Acta zoologica 32, 255–258.
Gouat, J. (1985). Notes sur la reproduction de Ctenodactylus gundi rongeur Jones, C. B. (2005). Behavioral flexibility in primates. Causes and consequences.
Ctenodactylidae. Zeitschrift für Säugetierkunde 50, 285–293. Springer, New York.
Green, B. & Merchant, J. C. (1988). The composition of marsupial milk. In The Karim, K. B. & Gupta, N. (1986). A case of superfetation in the Indian Fruit bat,
Rousettus leschenaulti (Desmarest). Bat Research News 27, 13–14.
Developing Marsupial: Models for Biomedical Research. (eds: Tyndale-Biscoe and P. A.
Kemkes, H. (1922). Ein Beitrag zum Problem der Superfoetatio. Dissertation, Würzburg.
Janssens), pp. 41–54. Springer, Berlin.
King, H. D. (1913). Some anomalies in the gestation of the albino rat (Mus norwegicus
Green, B., Merchant, J. C. & Newgrain, K. (1988). Milk consumption and
albinos). Biological Bulletin 24.
energetics of growth in pouch young of the tammar wallaby, Macropus eugenii.
Klemme, I., Ylönen, H. & Eccard, J. A. (2008). Long-term fitness benefits of
Australian Journal of Zoology 36, 217–228.
polyandry in a small mammal, the bank vole Clethriomys glareolus. Proceedings of the
Green, B., Newgrain, K. & Merchant, J. C. (1980). Changes in milk composition
Royal Society B 275, 1095–1100.
during lactation in the tammar wallaby (Macropus eugenii). Australian Journal of Biological Knaus, H. (1966). Zur Frage der Superfetation beim Feldhasen. Zeitschrift für
Sciences 33, 5–42. Jagdwissenschaften 12, 1–5.
Green, S. W. & Renfree, M. B. (1982). Changes in milk proteins during lactation Knaus, H. (1967). Zur Frage der Superfetation beim Feldhasen- Schlusswort. Zeitschrift
in the tammar wallaby, Macropus eugenii. Australian Journal of Biological Sciences 35, für Jagdwissenschaften 13, 52–53.
145–152. Kobayashi, F., Sagawa, N., Konishi, I., Tsuruta, Y., Fujiwara, H. & Mori, T.
Griffiths, M., McIntosh, D. L. & Leckie, R. M. C. (1972). The mammary glands (1996). Spontaneous conception and intrauterine pregnancy in a symptomatic missed
of the Red Kangaroo with observations on the fatty acid components of the milk abortion of ectopic pregnancy conceived in the previous cycle. Human Reproduction
triglycerides. Journal of Zoology 166, 265–275. 11, 1347–1349.
Haerer, G., Nicolet, J., Bacciarini, L., Gottstein, B. & Giacometti, M. Krehbiel, R. H. (1952). Mating of the golden hamster during pregnancy. The
(2001). Todesursachen, Zoonosen und Reproduktion bei Feldhasen in der Schweiz. Anatomical Record 113, 117–121.
Schweizerisches Archiv für Tierheilkunde 143, 139–201. Kroon, R. H. (1829). Superfetation bei einer Ziege. Tigdschrift voor Nekartenskunde.
Hall, W. H. (1987). Short communication: Bovine superfetation by natural Kuntz, A. (1920). Retention of dead fetuses in utero and its bearing on the problems
conception secondary to an embryo transfer pregnancy. Cornell Veterinarian 77, of superfetation and superfecundation. The Anatomical Record 18, 295–307.
282–283. Kussmaul, A. (1859). Von dem Mangel, der Verkümmerung und der Verdoppelung
Hammond, J. Jr. (1951). Control by light of reproduction in ferrets and mink. Nature der Gebärmutter, von der Nachempfängnis und der Überwanderung des Eies.
167, 150–151. Würzburg.
Hansen, K. (1992). Reproduction in European hares in a Danish farmland. Acta Larivee, J. M. (1972). Superfetation chez une truie. Canadian Veterinarian Journal 13,
Theriologica 37, 27–40. 242–243.
Hansson, A. (1947). The physiology of reproduction in mink (Mustela vison, Schreb.) Lariviere, S. (1999). Mammalian species: Mustela vison. American Society of Mammalogists
with special reference to delayed implantation. Acta Zoologica 28, 1–136. 608, 1–9.
Hare, J. F., Todd, G. & Untereiner, W. A. (2004). Multiple mating results in Leakey, L. S. B. (1969). Presumed super-foetation in an Erythrocebus patas monkey.
multiple paternity in Richardson’s ground squirrels (Spermophilus richardsonii). Canadian Nature 223, 754.
Field Naturalist 118, 90–94. Lechleitner, R. R. (1959). Sex ratio, age classes and reproduction of the black-tailed
Harman, M. T. (1917). A case of superfetation in the cat. The Anatomical Record 13, jack rabbit. Journal of Mammalogy 40, 63–81.
145–157. Lemon, M. & Barker, S. (1967). Changes in milk composition of the Red Kangaroo
Harman, M. T. (1919). A probable case of superfetation in the cow. The Anatomical Megaleia rufa (Desmarest) during lactation. The Australian Journal of Experimental Biology
Record 14, 335–336. and Medical Science 45, 213–219.
Harrison, A., Valenzuela, A., Gardiner, J., Sargent, M. & Chessex, P. (2005). Leonard, A. & Linden, G. (1972). Superfoetation in CBA mice. Cellular and Molecular
Superfetation as a cause of growth discordance in a multiple pregnancy. Journal of Life Sciences 28, 159.
Pediatrics 147, 254–255. Licht, P. (1984). Reproductive cycles of Vertebrates—Reptiles. In Marshall’s physiology
Hartel, J. (1958). Doppelseitige Extrauteringravidität (Superfetatio?). Zentralblatt für of reproduction (ed. G. E. Lamming), 206–286. Churchill Livingstone, Edinburgh.
Gynäkologie 29, 1148–1150. Lienhardt, R. (1940). A propos de la durée de la gestation chez le lièvre. Comptes
rendus des seances de la societe de biologie et de ses filiales 1, 133–135.
Hediger, H. (1948). Die Zucht des Feldhasen (Lepus europaeus PALLAS) in
Lincoln, D. W. & Renfree, M. B. (1981). Mammary gland growth and milk ejection
Gefangenschaft. Physiologica comparata Oecologia 1, 46–63.
in the agile wallaby, Macropus agilis, displaying concurrent asynchronous lactation.
Hell, P., Flak, P. & Slamečka, J. (1997). Korrelation zwischen der
Journal of Reproduction & Fertility 63, 193–203.
Streckenentwicklung des Rot- und Rehwildes sowie des Feldhasen und ihrer
Lindenfors, P., Dalen, L. & Angerbjörn, A. (2003). The monophyletic origin of
wichtigsten Prädatoren in der Slowakei in den Jahren 1968–1995. Zeitschrift für
delayed implantation in carnivores and its implications. Evolution 57, 1952–1956.
Jagdwissenschaften 43, 73–84.
Littleford, R. A. & Gysin, H. A. (1944). Observations on superfetation in mice.
Hermes, R., Hildebrandt, T. B., Göritz, F., Jewgenow, K., Lengwinat, T. & The Anatomical Record 89, 507–513.
Hofmann, R. R. (2000). Ultrasonography of the ovaries and uterus and grey scale Lovell, R. (1661). A complete history of animals and minerals. Oxford.
analysis of the endometrium during embryonic diapause in European roe deer Markee, J. E. & Hinsey, J. C. (1935). A case of probable superfetation in the cat. The
(Capreolus capreolus). Acta Theriologica 45, 559–572. Anatomical Record 61, 241–251.
Hinrichs, K. & Watson, E. D. (1988). Clinical report: Recovery of a degenerating Martinet, L. (1980). Oestrus behaviour, follicular growth and ovulation during
14-day embryo in the uterine flush of a mare 7 days after ovulation. Theriogenology pregnancy in the hare (Lepus europaeus). Journal of Reproduction & Fertility 59, 441–445.
30, 349–353. Martinet, L., Legouis, J. J. & Moret, B. (1970). Quelques observations sur la
Hollander, W. F. (1960). Genetics in relation to reproductive physiology in reproduction du lièvre européen (Lepus europaeus PALLAS) en captivité. Annales de
mammals. Journal of Cellular & Comparative Physiology 56 (S1), 61–72. biologie animale, biochimie, biophysique. 10, 195–202.
Honore, L. H. & Nickerson, K. G. (1977). Combined intrauterine and tubal ectopic Martinet, L. & Raynaud, F. (1972). Méchanisme possible de la superfetation chez
pregnancy: A possible case of superfetation. American Journal of Obstetrics & Gynecology la hase. Comptes rendus de l’academie des sciences Paris 274, 2683–2686.
127, 885–887. Martinet, L. & Raynaud, F. (1973). Prolonged spermatozoan survival in the female
Hoogeweg, J. H. & Folkers, E. R. Jr. (1970). Superfetation in a cat. Journal of the hare uterus: Explanation of Superfetation. In The Biology of Spermatozoa. INSERM
American Veterinary Medical Association 156, 73–75. International Symposium, Nouzilly, pp. 134–144. Karger, Basel.
Hunt, H. R. (1919). Birth of two unequally developed cat fetuses (Felis domestica). The Matter, H. E. (1965). A case of superfetation in the karakul sheep. Berliner Münchner
Anatomical Record 16, 371–378. Tierärztliche Wochenschrift 78, 469–470.
Mayer, G. & Klein, M. (1946). Production d’une nouvelle gestation au cours d’une Renfree, M.B. (2009). Review: Marsupials: Placental mammals with a difference.
gravidite chez la lapine. Social Biology 140, 1011–1012. Placenta (In Press).
Meisner, A. D. (2001). Phylogenetic systematics of the viviparous halfbeak Renfree, M. B. & Shaw, G. (2000). Diapause. Annual Review of Physiology 62, 353–375.
genera Dermogenys and Nomorhamphus (Teleostei: Hemiramphidae:Zenarchopterinae). Reznick, D. N., Mateos, M. & Springer, M. S. (2002). Independent origins and
Zoological Journal of the Linnean Society 133, 199–283. rapid evolution of the placenta in the fish genus Poeciliopsis. Science 298, 1018.
Meisner, A. D. & Burns, J. R. (1997). Viviparity in the halfbeak genera Dermogenys Reznick, D., Meredith, R. & Collette, B. B. (2007). Independent evolution of
and Nomorhamphus (Teleotei: Hemiramphidae). Journal of Morphology 234, 295–317. complex life history adaptations in two families of fishes, live-bearing halfbeaks
Milne, I. A. (1956). A case of prolonged pregnancy and a review of the literature (Zenarchopteridae, Beloniformes) and Poeciliidae (Cypinodontiformes). Evolution
on superfoetation in an endeavour to explain the phenomenon. The Central African 61, 2570–2583.
Journal of Medicine 2, 385–389. Reznick, D. N. & Miles, D. B. (1989). Review of life history patterns in poeciliid
Mitchell-Jones, A. J., Amori, G., Boganowicz, W., Kryštufek, B., Reijnders, fishes. In Ecology and evolution of livebearing fishes (Poeciliidae) (eds. G. K. Meffe &
P. J. H., Spitzenberger, F., Stubbe, M., Thissen, J. B. M., Vohralík, V. & F. F. Snelson, Jr.), pp. 125–148. Prentice Hall.
Zima, J. (1999). The atlas of European mammals. Academic Press, London. Rieck, W. (1956). Untersuchungen über die Vermehrung des Feldhasen. Zeitschrift für
Mondain-Monval, M., Bonnin, M., Canivenc, R. & Scholler, R. (1980). Plasma Jagdwissenschaften 2, 49–90.
estrogen levels during delayed implantation in the European badger (Meles meles L.). Roberts, T. R. (1989). The freshwater fishes of Western Borneo (Kalimantan Barat,
General and Comparative Endocrinology 41, 143–149. Indonesia). Memoirs of the California Academy of Sciences 14, 1–210.
Mor, G. (2006). Immunology of pregnancy. Landes Bioscience/Eurekah.com, Robertson, S. A. (2005). The Seminal plasma and male factor signaling in the female
Georgetown. reproductive tract. Cell & Tissue Research 322, 43–52.
Myers, K., Parer, I. & Richardson, B. J. (1989). Leporidae. In Fauna of Australia. Robertson, S. A. (2007). Seminal fluid signaling in the female reproductive tract:
Mammalia. Volume 1B (eds. D. W. Walton & B. J. Richardson) pp. 917–931. Lessons from rodents and pigs. Journal of Animal Science 85, E36–44.
Australian Government Publishing Service, Canberra. Roellig, K., Fassbender, M., Goeritz, F., Slamečka, J. & Hildebrandt, T. B.
Nakagawa, H., Yoshinaga, K. & Hosi, T. (1966). On the parturition of the (2005). Evaluation of embryonic mortality in European brown hares (EBH) using
experimentally induced super-implanting rat. Japanese Journal of Animal Reproduction transcutaneous ultrasonography. Schweizerisches Archiv für Tierheilkunde 147, 72.
12, 66–69. Rollhäuser, H. (1949). Superfetation in a mouse. The Anatomical Record 105, 657–663.
Newsome, A. E. (1965). The influence of food on breeding in the red kangaroo in Rose, K. D., De Leon, V. B., Missiaen, P., Rana, R. S., Sahni, A., Singh, L. &
central Australia. Wildlife Research 11, 187–196. Smith, T. (2008). Early Eocene lagomorph (Mammalia) from Western India and
Neuhaus, L. (1954). Die biologischen Voraussetzungen der Superfetation der Frau. the early diversification of Lagomorpha. Proceedings of the Royal Society B London 275,
Enke, Berlin. 1203–1208.
Nicholas, K. R. (1988). Asynchronous dual lactation in a marsupial, the tammar Rosenberg, H. (1954). Mehrlingsschwangerschaft oder Superfötation? Zeitschrift für
wallaby (Macropus eugenii). Biochemical and Biophysical Research Communications 154, Tierärztliche Fortbildung 48, 629–631.
529–536. Rothchild, I. (2003). The yolkless egg and the evolution of eutherian viviparity.
Niethammer, J. & Krapp, F. (2003). Ordnung Lagomorpha - Hasentiere. In Handbuch Biology of Reproduction 68, 337–357.
der Säugetiere Europas. Bd. 3 (ed. F. Krapp). Aula, Wiebelsheim. Sackmann, H. J. (1977). Erfahrungen bei der Haltung des Feldhasen (Lepus europaeus
Nottle, F. K. (1976). Superfetation in a sow and a cow. Australian Veteterinary Journal PALL.). Beiträge zur Jagd- und Wildforschung 10, 267–276.
52, 298. Sadlier, R. M. (1965). Reproduction in two species of kangaroo (Macropus robustus
Nowak, R. M. (1991). Order Lagomorpha. In Walkers Mammals of the World 5th edition, and Megaleia rufa) in the arid Pilbara region of Western Australia. Proceedings of the
pp. 539–560. The John Hopkins University Press , Baltimore & London. . . Zoological Society of London 145, 239–61.
Otsu, S. (1973). The breeding and ecology of the Tohoku hare Lepus brachyurus Scanlon, P. F. (1960). An apparent case of superfoetation in a ewe. Australian Veterinary
angustidens HOLLISTER. Jikken Dobutsu, Supplements (0), 237–244. Journal 48, 74.
Ottow, B. (1952). Sondervorgänge in der Fortpflanzungsphysiologie der Säugetiere. Scanlon, P. F. (1972). Frequency of transuterine migration of embryos in ewes and
Säugetierkundliche Mitteilungen 1, 154–162. cows. Journal of Animal Science 34, 791–794.
Page, R. J. C., Ross, J. & Langton, S. D. (1994). Seasonality of reproduction in the Schäfers, G. (1996). Die Jagdstreckenentwicklung des Feldhasen (Lepus europaeus
European badger Meles meles in south-west England. Journal of Zoology 233, 69–91. PALLAS) von 1959 bis 1993 in der alten Bundesrepublik Deutschland in
Paplinska, J. Z., Moyle, R. L., Temple-Smith, P. D. & Renfree, M. B. (2006). Abhängigkeit von der Landwirtschaftsstruktur. Beiträge zur Jagd- und Wildforschung
Reproduction in female swamp wallabies. Reproduction, Fertility & Development 18, 21, 215–228.
735–43. Scrimgeour, J. B. & Baker, T. G. (1974). A possible case of superfetation in man.
Pickard, J. N. (1928). Cases of prolonged gestation, superfoetation and abnormal Journal of Reproduction & Fertility 36, 69–73.
pseudopregnancy in the rabbit. Veterinary Journal 84, 471–473. Scrimshaw, N. S. (1944). Superfetation in poeciliid fishes. Copeia 3, 180–183.
Pielowski, Z. (1971). Length of life in the hare. Acta Theriologica 16, 89–94. Shackelford, R. M. (1952). Superfetation in the ranch mink. The American Naturalist
Pielowski, Z. (1990). Über die Abhängigkeit der Besatzdichte und anderer 86, 311–319.
Populationsparameter des Hasen von der Agrarstruktur und landwirtschaftlichen Sharifi, M., Ghorbani, R., Fazeli, A. & Holt, W. (2004). Evidence of sperm
Aktivitäten. Beiträge zur Jagd- und Wildforschung 17, 156–162. storage in Pipistrellus kuhlii (Chiroptera: Vespertilioniodae) in western Iran. Folia
Poduschka, W. (1996). Hyperthelie, Wurfgröße und Trächtigkeitsdauer bei der Zoologica 53, 1–6.
Unterfamilie Tenrecinae Cabrera, 1925 (Mammalia: Insectivora: Tenrecidae), nebst Sharman, G.B. & Calaby, J.H. (1964). Reproductive behaviour in the Red
Bemerkungen zur Längsstreifung der Gattung Hemicentetes. Contributions to Zoology 66, Kangaroo, Megaleia rufa, in captivity. CSIRO Wildlife Research 9, 58–85.
119–128. Sharman, G. B. & Pilton, P. E. (1964). The life history and reproduction of the red
Prakash, I. & Taneja, G. C. (1969). Reproduction biology of the Indian desert hare kangaroo, Megaleia rufa. Proceedings of the Zoological Society of London 142, 29–48.
(Lepus nigricollis dayanus Blanford). Mammalia 33, 102–117. Sharp, D. C. (1998). Horses. In Encyclopedia of Reproduction, Vol. 2. (eds: E. Knobil &
Quinn, P. J., Carter, M. E., Markey, B. & Carter, G. R. (1999). Section 6: J. P. Neill), 798. Academic Press, San Diego.
A systems approach to infectious diseases on a species basis. In Clinical Veterinary Shepherd, J. (1998). Sperm Activation, Arthropods. In Encyclopedia of Reproduction,
Microbiology, p. 540. Mosby, Edinburgh. Vol. 4. (eds: E. Knobil & J. P. Neill), 680–693. Academic Press, San Diego.
Raczynski, J. (1964). Studies on the European hare: V Reproduction. Acta Theriologica Shivaji, S. & Bhargava, P. M. (1987). Antifertility Factors of Mammalian Seminal
9, 305–352. Fluid. BioEssays 7, 13–17.
Ramaswami, L. S. & Anand Kumar, T. C. (1963). Differential implantation of twin Short, C. E. (1964). Superfetation in a burro. Journal of the American Veterinary Medical
blastocysts in Megaderma (Microchiroptera). Experientia 19, 641–642. Association 144, 257–258.
Rao, K. S., Rao, E. R. & Sivaiah, K. (1987). Superfetation in a non-descript buffalo Sidorovich, V. E. (1993). Reproductive plasticity of the American mink (Mustela
heifer. Indian veterinary journal 64, 798. vison) in Belarus. Acta Theriologica 38, 175–183.
Rasweiler, J. J. (1982). The contribution of observations on early pregnancy on Singhal, S. R., Agarwal, U., Sharma, D. & Sen, J. (2003). Superfetation in uterus
the little sac-winged bat, Peropteryx kappleri to an understanding of the evolution of pseudo didelphys: an unreported event. Archives of Gynecology & Obstetrics 268,
reproductive mechanisms in monovular bats. Biology of Reproduction 27, 681–702. 243–244.
Renfree, M. B. (1983). Marsupial reproduction: the choice between placentation and Slagle, T. A., Oliphant, M. & Gross, S. J. (1989). Cingulate sulcus development
lactation. In Oxford Review of Reproductive Biology Vol. 5 (ed. C. A. Finn), pp. 1–29. in preterm infants. Pediatric Research 26, 598–602.
Oxford University Press, Oxford. Slamečka, J. & Šebová, K. (1991). Reproductive parameters of brown hare kept in
Renfree, M. B. (1993). Chapter 2: Ontogeny, Genetic Control, and Phylogeny of captivity. In XXth Congress of the International Union of Game Biologist. (eds. S. Csányi and
Female Reproduction in Monotreme and Therian Mammals. In Mammal Phylogeny; J. Ernhaft), pp. 618–627. University of Agricultural Sciences, Gödöllö, Hungary.
Mesaozoic Differentiation, Multituberculates, Monotremes, Early Therians, and Marsupials Slonaker, J. R. (1934). Superfetation in the albino rat. American Journal of Physiology
(eds. F. S. Szalay et al.), pp. 5–20. Springer, New York. 108, 322–323.
Smith, A. D. B. (1927). Superfoetation - Further cases in pigs and sheep. Journal of Tyndale-Biscoe, H. & Renfree, M. B. (1987). Breeding biology of marsupials
Anatomy 62, 100–104. by family. In Reproductive Phsysiology of Marsupials, pp. 14–95. University Press,
Smith, R., Mesiano, S. & Mc Grath, S. (2002). Hormone trajectories leading to Cambridge.
human birth. Regulatory Peptides 108, 159–164. van Dam, P. A., Vanderheyden, J. S. & Uyttenbroeck, F. (1988). Application of
Soong, M. H. H. (1968). Aspects of reproduction in freshwater halfbeaks. The Malayan ultrasound in the diagnosis of heterotopic pregnancy- a review of the literature.
Nature Journal, Supplements 21, 33–34. Journal of Clinical Ultrasound 16, 159–165.
Soudre, G., Guettier, X., Marpeau, L., Larue, L., Jault, T. & Barrat, J. Vandeplassche, M. (1969). The physiological explanation of split parturition in the
(1992). In utero early suspicion of superfetation by ultrasound examination: a case pig and other mammalian species. Annals of Endocrinology 30, 328–341.
report. Ultrasound in Obstetrics & Gynecology 2, 51–54. Venge, O. (1959). Reproduction in the fox and mink. Animal breeding abstracts 27,
Sparrow, S. (1977). Naturally occuring superfoetation in a rat. Laboratory Animals 11, 129–145.
49–50. Walter, A., Hasenohr, G. & Kerin, J. F. P. (1975). Superfetation in man. Australian
Sperling, O. (1926). Superfetatio et Superfecundatio. Dissertation, München. & New Zealand Journal of Obstetrics & Gynaecology 15, 240–246.
Starck, D. (1965). Superfecundation und Superfetatio. In Embryologie. Ein Lehrbuch auf Wandrey, R. (1977). Ein Fall von Superfötation bei Robben? Aus dem Ruhr-Zoo
allgemein biologischer Grundlage, 257–258. Georg Thieme, Stuttgart. Gelsenkirchen 53.
Stavy, M. & Terkel, J. (1992). Interbirth interval and duration of pregnancy in Watzka, M. (1959). Superfecundatio und Superfetatio. In Handbuch der Zoologie. Bd. 8,
hares. Journal of Reproduction & Fertility 95, 609–615. 23. Lieferung, (eds. J. G. Helmcke, H. Lengerken, D. Starck & H. Wermuth),
Steck, T. & Bussen, S. (1997). Conception during pregnancy (superfetation). Human pp. 2–6. Walter de Gruyter & Co., Berlin.
Reproduction 12, 1835–1836. Weichert, C. K. (1942). A case of parallel embryonic development in the rat and its
Stieve, H. (1952). Zur Fortpflanzungsbiologie des europäischen Feldhasen (Lepus bearing on the question of superfetation. The Anatomical Record 83, 511–519.
europaeus PALLAS). Zoologischer Anzeiger 148, 101–114. Weir, B. J. (1973). Another hystricomorph rodent: keeping casiragua (Proechymis guariae)
Stieve-Miegel, B. (1955). Über Superfetation bei der Bisamratte (Ondatra zibetica) in captivity. Laboratory Animals 7, 125–134.
(Superfetation in the muskrat). Zeitschrift für Mikroskopische und Anatomische Forschung Weir, B. J. (1974). Reproductive characteristics of hystricomorph rodents. Symposia of
61, 82–92. the Zoological Society of London 34, 265–301.
Stölting, K. N. & Wilson A. B. (2007). Male pregnancy in seahorses and pipefish: Weir, B. J. & Rowlands, I. W. (1973). Reproductive Strategies of Mammals. Annual
beyond the mammalian modell. BioAssays 29, 884–896. Review of Ecology and Systematics 4, 139–163.
Stowell, R. E. (1941). A case of probable superfetation in a mouse. The Anatomical Wislocki, G. B. & Snyder, F. F. (1931). On the experimental production of
Record 81, 215–220. superfetation. Johns Hopkins Hospital Bulletin 49, 103–105.
Takeda, Y., Torii, H. & Aiko, S. (1994). Reproductive traits of the captive Japanese Wozencraft, W. C. (2005). Family Mustelidae. In Mammal species of the world: A
hares Lepus brachyurus in Central Japan. Journal of the Mammological Society of Japan 19, taxonomic and geographic reference, 3rd edition (eds. D. E. Wilson & D. M. Reeder),
83–88. pp. 601–605. The Johns Hopkins University Press, Baltimore, Maryland.
Thibault, R. E. & Schultz, R. J. (1978). Adaptations among viviparous fishes Yamaguchi, N., Dugdale, H. L. & Macdonald, D. W. (2006). Female receptivity,
(Cyprinodontiformes: Poeciliidae). Evolution 32, 320–333. embryonic diapause, and superfetation in the European badger (Meles meles):
Thom, M., Johnson, D. & Macdonald, D. (2004). The evolution and maintenance implications for the reproductive tactics of males and females. Quarterly Reviews
of delayed implantation in the mustelidae (mammalia: carnivora). Evolution 58, of Biology 81, 33–48.
175–183. Yamaguchi, N., Sarno, R. J., Johnson, W. E., O’Brien, S. J. & Macdon-
Tocchini, M., Fronte, B., Nelli, G., Fichi, G. & Dimatteo, S. (2000). ald, D. W. (2004). Multiple paternity and reproductive tactics of free-ranging
Osservazioni sul fenomeno della superfetazione nella lepre in condizioni di minks, Mustela vison. Journal of Mammalogy 85, 432–439.
allevamento in cattivita (Observations about the phenomenon of the superfetation of Yoshinaga, K. (1961). Effects of local application of ovarian hormones on the delay
the hare in captivity). Annali Della Facolta Di Medicina Veterinaria Di Pisa 2000, 79–84. in implantation in lactating rats. Journal of Reproduction & Fertility 2, 35–41.
Töpfer-Petersen, E., Petrunkina, A., Ehklasi-Hundrieser, M. & Waber- Yoshinaga, K. (1971). The role of the fetus in the onset of partuition in the rat. The
ski, D. (2003). Funktion des weiblichen Spermienreservoirs beim Säugetier. Repro- Physiologist 14, 257.
duktionsmedizin 19, 173–180. Youngman, P. (1990). Mustela lutreola. Mammalian Species 362, 1–3.
Trexler, J. C. & De Angelis, D. L. (2003). Resource allocation in offspring Zörner, H. (1980). Zur Anzahl der Embryonen in den Uterushörnern und die Lage
provisioning: an evaluation of the conditions favoring the evolution of matrotrophy. der Foeten im Uterus beim Feldhasen (Lepus europaeus, PALLAS 1778). Beiträge zur
The American Naturalist 162, 574–585. Jagd- und Wildforschung 11, 325–334.
Tuppen, G. D., Fairs, C., de Chazal, R. C. & Konje, J .C. (1999). Spontaneous Zúñiga-Vega, J. J., Reznick, D. N. & Johnson, J. B. (2007). Habitat predicts
superfetation diagnosed in the first trimester with successful outcome. Ultrasound in reproductive superfetation and body shape in the livebearing fish Poeciliopsis
Obstetrics & Gynecology 14, 219–221. turrubarensis. Oikos 116, 995–1005.
Turner, C. L. (1937). Reproductive cycles and superfetation in poeciliid fishes. Zurowski, W. & Doboszynska, T. (1975). Superfoetation in European Beaver. Acta
Biological Bulletin 72, 145–164. Theriologica 20, 97–104.

Superfetation Mammals

Uploaded by

Copyright:

Available Formats

You might also like

Superfetation Mammals

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Superfetation Mammals

Uploaded by

Copyright:

Available Formats

Biol. Rev. (2011), 86, pp. 77–95.

The concept of superfetation: a critical review

(Received 26 May 2009; revised 10 March 2010; accepted 16 March 2010)

III. Clarification of reproductive phenomena often mistaken for superfetation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82

I. INTRODUCTION from marsupials to man (Table 1). These reports seldom

Subclass Taxonomic name Evidence for SF References Add Poss

Subclass Taxonomic name Evidence for SF References Add Poss

(3) Laboratory species

Order SF Other features of maternal care Reference

VII. DISCUSSION pregnancy. In mammals pregnancy is considered to be viable

TRUE SF: ACCIDENTAL SF:

Regular: Extremely rare:

Shortened interbirth Fetuses of different size; offspring

Superconception Superfertilization Superfetation proper

(F = fertilization; I = implantation; P = parturition)

You might also like