Reproductive biology and implications for management of the painted sweetlips Diagramma pictum in the southern Arabian Gulf

The reproductive biology of the painted sweetlips Diagramma pictum was determined from 487 individuals collected between January and December 2010 in the southern Arabian Gulf. There was no evidence of sex change and the combination of histological results with the sex composition of the size and age structures indicated a gonochoristic sexual pattern. There were peaks in gonado-somatic indices for females in March and October with spawning occurring during two seasons (April to May and November). The mean size and age at sexual maturity (L(m50) and A(m50) ) were 35·7 cm fork length (L(F) ) and 2·9 years for females and 26·7 cm L(F) and 0·5 years for males. The maximum recorded age (11 years) and small mean size and young age at sexual maturity for males may be a direct result of intensive demersal fishing in the southern Arabian Gulf. There was an exponential increase in the cumulative reproductive potential with size and a linear increase with age for both sexes. The mean L(F) (L(c50) ) at which D. pictum became vulnerable to capture was 33·3 cm, which corresponded to only 3 and 7% of the cumulative reproductive potential of males and females, respectively. Size-specific and age-specific reproductive potential indicated that conventional regulations that equate the mean size at first capture to sexual maturation are unsuitable for the management of D. pictum.     

Seasonal changes of progesterone and testosterone concentrations throughout gonad maturation stages of the Mexican octopus,Octopus maya (Octopodidae: Octopus)

Variations in progesterone (P₄) and testosterone (T) levels in the gonad of Octopus maya from Sisal in Yucatan State, Mexico, were investigated by radioimmunoassays and in relation to four gonad maturation stages (GMS) and to the reproductive cycle, as represented by two maturity indices (microscopic ‘MiMI’ and macroscopic ‘MaMI’). According to the GMS and the maturity indices, the reproductive season of O. maya from Yucatan occurred from February to June. In females, P₄ and T displayed the same pattern, with a tendency to increase at the same time, although on average, P₄ had seven-fold higher concentrations than T. In contrast, P₄ and T in male gonads displayed a different pattern, where T concentrations were relatively stable throughout all of the study months. In the female gonad P₄ was lowest (close to 0 pg?g^–1) during both developing (GMS-I) and maturing (GMS-II) stages, and increased (189?±?53?pg?g^–1) approaching the mature stage (GMS-III) to a maximum value of 611?pg?g^–1. Concentrations of T in the male gonad were lowest (106?±?9?pg?g^–1) during the maturing stage (GMS-II) and increased up to the mature stage (GMS-III), reaching a maximum of 440?pg?g^–1. Pearson's correlation (r) between hormones and maturity indices showed strong relationships for females (around 0.4 and ?0.7; p?<?0.05), but there were negligible or weak relationships for males (0.2 and ?0.1; p?>?0.05). Hormone correlations in females were inverse with MaMI and direct with MiMI. Our major findings showed that gonadal P₄ levels were elevated during GMS-III and GMS-IV (i.e. periods of vitellogenic oocytes), where the characteristic aspect is an ovary with very high oocyte diameters, with the primary follicle cells deeply infolded in the ooplasm for yolk synthesis. These results suggested a synchrony between P₄ and the process of folliculogenesis, and in turn, vitellogenesis.     

Reproductive biology of the prawn Melicertus kerathurus (Decapoda: Penaeidae) in Thermaikos Gulf (N. Aegean Sea)

The reproductive biology including insemination frequency, ovarian maturation, gonadosomatic index (GSI), size at first maturity, and fecundity of Melicertus kerathurus were investigated using monthly samples from Thermaikos Gulf. Insemination was recorded by the presence of a spermatophore in the thelycum, and ovarian development was based on macroscopic ovarian staging (ST1–ST5). Inseminated females were found throughout the year with high percentages recorded from April to July. Although all ovarian stages were represented in mated females, insemination increased with size and ovarian maturation. High percentages of vitellogenic or mature ovarian stages were observed from May to July, while immature and developing ovaries were predominant mainly in winter. Spawned ovaries occurred from May to October. Carapace length at first maturity based on the presence of a spermatophore (CL_50sp) was estimated at 39.20 mm, while that based on the presence of vitellogenic and mature ovaries (CL_50ov) at 40.70 mm. The seasonal peak in the proportion of mature females (ST4) varied with size. Inseminated females at ST4 and GSI peaked in June–July. GSI varied in relation to insemination status and ovarian stage. In large females (>50 mm CL), the decline in mature ovaries and GSI increment with size indicates a relative reduction in the reproductive output. The number of oocytes ranged from 62,742 to 602,947 (mean ± SD: 268,000 ± 113,000). As the prawns are targeted during the spawning season, mainly by the artisanal fishery, and female size at first maturity is selected by artisanal net size, managerial measures toward artisanal fishery should be implemented.     

Reproductive biology and implications for management of the spangled emperor Lethrinus nebulosus in the southern Arabian Gulf

The reproductive biology of the spangled emperor Lethrinus nebulosus in the southern Arabian Gulf was determined from the examination of 781 individuals collected between September 2008 and August 2009. There was no histological evidence of adult sex change, and sex ratios did not differ significantly from unity across all size and age classes. Testes had an ovarian structure and a remnant lumen which was not used for sperm transport; furthermore, residual oocytes were observed in the testes of some immature, resting and developing males. A dramatic change in the sex ratio of the smallest and youngest size and age classes suggested that juvenile female to male sex change occurred between 21·0 cm fork length (L(F)) and 24·0 cm L(F) at 1 year of age. The combination of histological evidence with the sexual composition of the size and age structures suggests a non-functional protogynous hermaphroditic sexual pattern, which is analogous to functional gonochorism. The spawning season was well defined, occurring once a year during March, April and early May. Peaks in spawning occurred after full moons, there was a cessation in spawning activity after new moons and spawning was completed within three lunar cycles. The distribution of males over the entire size and age ranges and the absence of inactive mature females during the spawning season suggested that the population was not constrained by sperm limitation. Size-specific and age-specific reproductive potential indicated that conventional regulations that equate the mean size at first capture to sexual maturation are unsuitable for the management of L. nebulosus. The maximum recorded age (11 years), small mean size and young age at sexual maturation (L(m50) = 26·7 cm L(F), 2·1 years, for females and 19·4 cm L(F), 0·5 years, for males) may be a direct result of intensive demersal fishing in the southern Arabian Gulf.     

Reproductive biology of Bagrus docmak in the Victoria Nile,Uganda

Aspects of the reproductive biology of Bagrus docmak in the Victoria Nile were investigated between November 2005 and October 2006. Macroscopic and histological analysis of the gonads confirmed it as an asynchronous batch spawner which spawns throughout the year with bimodal spawning peaks coinciding with rainfall seasons. The first spawning peak occurred from March to May, the second from September to November. The sex ratio did not significantly deviate from 1:1. Length at sexual maturity was 33.6 cm and 31.6 cm fork length (FL) for females and males, respectively. Batch fecundity ranged from 1 000 eggs in 34 cm FL fish to 43 000 eggs in 79 cm FL fish, and correlated linearly with FL (r = 0.72) and body weight (r = 0.79). Mean relative batch fecundity was 6 eggs g^?1 (SE 2). These results could guide research into the possibility of artificially inducing the fish to spawn, and its subsequent culture.     

Reproductive biology of Carcharhinus acronotus in the coastal waters of South Carolina

The reproductive biology of blacknose sharks Carcharhinus acronotus in the western North Atlantic Ocean was studied by examining specimens collected in the coastal waters of South Carolina. Males begin the maturation process between 875 and 910 mm fork length ( L _F), as indicated by the presence of functional claspers and siphon sacs. The presence of vitellogenic oocytes and developing oviducal glands and uteri indicated that females begin to mature at c . 870 mm L _F. Length at which 50% of the population reached maturity was 896 and 964 mm L _F, equivalent to 4·3 and 4·5 years, for males and females, respectively. Gonado‐somatic indices suggested that spermatogenesis and vitellogenesis began after December. Mating took place during the end of May and the beginning of June. Fertilization occurred during late June and early July, suggesting that female blacknose sharks were capable of sperm storage. Based on the timing of fertilization and occurrence of females carrying near‐term pups in late May and early June, the gestation period for blacknose sharks was c . 11 months. Female blacknose sharks reproduced biennially based on the absence of vitellogenic oocytes in near‐term females and there being no indication of vitellogenesis in postpartum females. Male blacknose sharks were capable of reproducing annually as indicated by turgid genital ducts, which were observed in all mature males collected during late May and early June.     

Reproductive biology of the fanray, <Emphasis Type="Italic">Platyrhina sinensis</Emphasis> (Batoidea: Platyrhinidae) in Ariake Bay,Japan

The reproductive biology of the fanray, Platyrhina sinensis, was examined in Ariake Bay, Japan, from May 2002 until December 2006. Females reached sexual maturity at a larger size than males [total length (TL) at 50% sexual maturity: male, 393 mm; female, 421 mm]. The present data support a distinct annual reproductive cycle for P. sinensis. The gonadosomatic index (GSI) for mature males showed a clear seasonal trend, declining from August to November. Histological observations showed that mature sperm in the testes occurred from August to November when monthly GSI declined. Concomitantly, pre-ovulatory ova were observed in females collected from August to November. These data indicate that mating, ovulation and fertilization occurred from August to November. Near-term embryos, neonates and recent post-partum females also occurred from August to November. Additionally, all post-partum females possessed large pre-ovulatory ova. Parturition occurred from August to November followed immediately by mating, ovulation and fertilization. Mature females become pregnant every year, and the gestation period is almost 1 year. Fertilized uterine eggs without macroscopic embryonic development were present throughout the annual reproductive cycle, indicating that P. sinensis utilizes embryonic diapause as its reproductive strategy. Both reproductive tracts of females were functional, and fecundity ranged from 1 to 12 with a mean of 6.0, increasing with TL.     

The influence of feeding regime on sexual maturation, fecundity and atresia in first-time spawning turbot

Exposure of adolescent turbot Scophthalmus maximus to low rations during vitellogenesis, covering the 4 months immediately prior to spawning, led to a drop of 70% in mean ovary weight, and was associated with poor growth of the vitellogenic oocytes or, in a third of cases, the absence of vitellogenic oocytes. Exposure to low rations during the recruitment of vitellogenic oocytes, 4–8 months prior to spawning, produced a more variable response. A few of these females produced well-developed vitellogenic oocytes, but in most, vitellogenic oocytes were absent or only poorly developed and in some cases there was a high incidence of atresia. Exposure to intermediate rations throughout oocyte recritment and vitellogenesis also depressed oocyte development. In maturing females the number of non-atretic vitellogenic oocytes (relative potential fecundity) averaged 998 per g of somatic body weight of fish at the start of the spawning season in mid-June. Maturation of the males was not significantly influenced by the dietary regime. The small size of the testes and the low levels of milt production, even in fish fed high rations immediately prior to spawning, showed that reproductive investment in males was much lower than in females.     

Spawning season and size at sexual maturity of <Emphasis Type="Italic">Kyphosus bigibbus</Emphasis> (Kyphosidae) from northwest Kyushu,Japan

The reproductive characteristics of Kyphosus bigibbus were examined using individuals collected between June 2004 and February 2009 off Nagasaki Peninsula in northwest Kyushu, Japan. The spawning season and size at sexual maturity of this species were characterized based on a gonad index and histological examination of the gonads. The spawning season extends from June to October. This species is assumed to be an indeterminate, multiple-batch spawner. Females reached sexual maturity at larger size than males (fork length at 50% sexual maturity: males 284 mm, females 360 mm).     

Annual reproductive cycle,spawning periodicity and sexual maturity of blue runner Caranx crysos (Pisces,Carangidae) from the Gulf of Gabes (Tunisia,Eastern Mediterranean)

From June 2004 to May 2006, the reproductive biology of the blue runner Caranx crysos was studied in the Gulf of Gabes (Southern Tunisia). Of 1668 individuals examined, 777 were females (46.6%) and 891 were males (53.4%). The sex ratio significantly deviated in favour of males (♀:♂ = 0.87 : 1). The difference in the numbers of females and males was significant among size‐classes. However, there was no significant difference between sexes over months and seasons. Monthly changes in the Gonado‐Somatic Index (GSI) showed a rapid increase during summer to very high levels in July (3.51% for males and 2.55% for females) and August (3.47% for males and 2.59% for females) before declining sharply in September (0.58% for females and 0.38% for males). The gametogenesis activity began with a pre‐maturation phase, from 20 May to the first 10 days of July, followed by a pre‐spawning phase, from 20 July to 20 August. From the last 10 days of August to 20 September the gonads were in the ripe and spawning stages. From the end of September to early May, gonads were in the post‐spawning and resting stages. The size at which 50% of the population reached sexual maturity was significantly different in males and females: males attained sexual maturity at fork length FL₅₀ = 210.20, whereas females attained maturity at FL₅₀ = 222.3 mm. Age at maturity was 2.4 years for males and 2.8 years for females.     

Reproductive biology of female striped marlin Kajikia audax in the western Pacific Ocean

Length and mass data for 1260 (536 females, 683 males, 41 sex unknown) striped marlin Kajikia audax were collected at the fish markets of Tungkang, Singkang and Nanfangao from July 2004 to September 2010. Of these samples, 534 gonads (236 females and 298 males) ranging from 95 to 206 cm in eye‐to‐fork length (L _EF ) and 8 to 88 kg in round mass (M _R), were collected. Chi‐square tests indicated sex ratios were homogeneous among months in 2004 and 2006–2008, but not in 2005, 2009 and 2010; and there were significant differences in sex ratio by size. The overall sex ratio (R _S ) differed significantly from the expected 0·5. Kajikia audax are sexually dimorphic and the proportions of females increased with size between 140 and 210 cm L _EF . Reproductive activity was assessed using a gonado‐somatic index (I _G ), external appearance of the gonads and histological examination and results indicated that the spawning season occurred from April to August with a peak in June to July. Based on histological observations and the distribution of oocyte diameters, K. audax are multiple spawners and their oocytes develop asynchronously. The estimated length‐at‐50% maturity (L _EF50 ) was c . 181 cm (c . 4·8 years of age) for females. The proportion of reproductively active females in the spawning season with ovaries containing postovulatory follicles (0·27) indicated that they spawned every 3·7 days on average. The hydrated oocyte method estimated mean ± S.D. batch fecundity (F _B ) to be 4·4 ± 2·02 million eggs; average relative fecundity was 53·6 ± 13·9 oocytes g^?1 M _R; and the average annual fecundity was 181·3 ± 48·3 million eggs. The parameters estimated in this study are key information for stock assessments of K. audax in the north‐western and central Pacific and will contribute to the conservation, management and sustainable yield of this species.     

Annual reproductive cycle,spawning periodicity and sexual maturity of false scad Caranx rhonchus (Geoffroy Saint‐Hilaire, 1817) (Pisces,Carangidae) from the South‐Eastern Mediterranean (Gulf of Gabès,Tunisia)

The reproductive biology of Caranx rhonchus (Geoffroy Saint‐Hilaire, 1817) (Pisces, Carangidae) was studied in the Gulf of Gabès (Mediterranean Sea) from June 2004 to May 2006. Of 1313 individuals examined, 668 were females (50.9%) and 645 were males (49.1%). The overall sex ratio did not deviate significantly in favour of females (♀ : ♂ = 1.04 : 1). Monthly changes in the Gonado–Somatic Index (GSI) showed a rapid increase from May to June and an extended very high level from June to September (4.43–3.47% for females and 3.35–2.61% for males), before declining sharply in October (down to 2.02% for females and 0.57% for males). The gametogenesis activity began with a pre‐maturation phase from March to May, followed by a ripe‐spawning phase from June to September. From the last days of July to the end of October, the gonads were in the spent and post‐spawning stages. From November to early May, gonads were in the resting stages. The size at which 50% of the population reached sexual maturity was not significantly different between males and females :  males attained sexual maturity at fork length FL₅₀ = 161.20 ± 0.37 mm (n = 262), whereas females attained maturity at FL₅₀ = 160.70 ± 0.23 mm (n = 296). The age of maturity for both sexes occurred at 2.1 years.     

Reproductive seasonality of the detritivorous fish <Emphasis Type="Italic">Cyphocharax abramoides</Emphasis> (Kner, 1958) (Characiformes: Curimatidae) in flooded rivers of the eastern Amazon

The Lower Anapu River, Eastern Amazon, has a discrete flood pulse with narrow flooded areas due to the reduced influence of tides. In this environment, local precipitation might act as an important factor in the input of detritus, which can serve as a trigger for fish reproductive period. Therefore, this paper aims to determine the effects of local precipitation on the reproductive ecology of an abundant detritivorous fish in flooded rivers. Between May 2012 and April 2013, 886 specimens (471 females and 415 males) were captured monthly using gill nets. Individuals were measured, weighted, sexed, and the gonadal development stage was defined macroscopically and confirmed histologically. Sex ratio, length-weight relationship (LWR), condition factor (k), Gonadosomatic Index (GSI), relative frequency of maturity stages, and size at first gonadal maturity (L₅₀) were estimated and tested in relation to rainfall periods. There was no difference between the expected sex ratio (1:1), and both males and females showed polyphasic growth. The condition factor indicated higher values at the beginning of the rainy season and lower values during the dry season for both sexes. GSI and relative frequency of mature individuals indicated a long reproduction period with gonadal investment starting within the dry season until early in the rainy season for spawning within the rains. The L₅₀ value showed that males reach sexual maturity before females. Results indicated a reproductive pattern strongly influenced by rainfall, corroborating the importance of local precipitation for lacustrine environments.     

Maturation and sexual ontogeny in the spangled emperor Lethrinus nebulosus

The reproductive development and sexual ontogeny of spangled emperor Lethrinus nebulosus populations in the Ningaloo Marine Park (NMP) were investigated to obtain an improved understanding of its evolved reproductive strategy and data for fisheries management. Evidence derived from (1) analyses of histological data and sampled sex ratios with size and age, (2) the identification of residual previtellogenic oocytes in immature and mature testes sampled during the spawning season and (3) observed changes in testis internal structure with increasing fish size and age, demonstrated a non‐functional protogynous hermaphroditic strategy (or functional gonochorism). All the smallest and youngest fish sampled were female until they either changed sex to male at a mean 277·5 mm total length (L_T) and 2·3 years old or remained female and matured at a larger mean L_T (392·1 mm) and older age (3·5 years). Gonad masses were similar for males and females over the size range sampled and throughout long reproductive lives (up to a maximum estimated age of c. 31 years), which was another correlate of functional gonochorism. That the mean L_T at sex change and female maturity were below the current minimum legal size (MLS) limit (410 mm) demonstrated that the current MLS limit is effective for preventing recreational fishers in the NMP retaining at least half of the juvenile males and females in their landed catches.     

Reproduction of the duck catfish Ageneiosus ucayalensis in a ria river system

A total of 1006 duck catfish Ageneiosus ucayalensis were collected from a ria river system of eastern Amazonia, of which 733 were females and 273 males, a sex ratio 2·69:1. Condition factors of males were higher than those of females and size at first sexual maturity (L₅₀) was 12·8 cm for females and 11·8 cm for males. The relative frequency of mature specimens and gonad condition indices indicate that the breeding season is short and coincides with the rainy season.     

The reproductive biology of Plagioscion squamosissimus (Heckel, 1840) in the Pará River estuary (Amazon Estuary)

This study describes the reproductive biology of the South American silver croaker Plagioscion squamosissimus (Heckel, 1840) in the Pará River estuary. Data were collected bimonthly from June 2007 to May 2008. In all, 334 specimens were examined. The gonads were processed with histological techniques, and the ovaries were subjected to morphometric analysis. The length at first maturity (L₅₀) values were 16.14 and 21.43 cm total length for females and males, respectively. The sex ratio based on the total number of individuals favoured the females (1.11 females: one male). Macroscopically, the gonads were classified as immature (A), maturing (B), mature (C) and spent (D). Microscopically, four germ cell types were distinguished based on the development of the ovaries. Chromatin nucleolus (I), perinucleolar (II), cortical alveoli (III) and full‐vitellogenic (IV) oocytes were observed in all ovarian stages, except that of the mature individuals which showed the largest number of full‐vitellogenic oocytes (IV), with a mean diameter of 565.4 μm (±147.4). Substantial percentages of individual P. squamosissimus were found to be in a reproductive condition. Reproductive activity was recorded throughout the year in the Pará River estuary, primarily in February/March and August/September.     

Reproductive biology of the guitarfish <Emphasis Type="Italic">Rhinobatos hynnicephalus</Emphasis> (Batoidea: Rhinobatidae) in Ariake Bay,Japan

Size at sexual maturity, reproductive cycle, and fecundity of the guitarfish, Rhinobatos hynnicephalus, were examined in Ariake Bay, Japan. Females reached sexual maturity at a larger size than males [total length (TL) at 50% sexual maturity: males, 431 mm; females, 476 mm]. Monthly gonadosomatic indices of males decreased abruptly from July to August. Histological examinations confirmed the presence of mature spermatozoa in the testes in July, with semen in seminal vesicles in July and August. Preovulatory ova were observed in females with near-term embryos in August. Parturition occurred in August, immediately followed by mating, ovulation, and fertilization. Gestation period is approximately 1 year. Fertilized uterine eggs without embryonic development were present throughout the annual reproductive cycle. Embryonic development began in June and ended in August, indicating that R. hynnicephalus undergoes embryonic diapause (9 months). Fecundity increased with TL and ranged from 1 to 9 (mean, 4.4) embryos per litter.     

Size at the onset of sexual maturity in the anomuran crab, Aegla uruguayana (Aeglidae)

The size at maturity was studied in the crab Aegla uruguayana from the Areco River (31°14′ S, 59°28′ W), Argentina. Size at sexual maturity was determined according to three criteria: morphometric (change in the relative growth of reproductive characters), histological (first maturation of gonads) and functional (capability to mate and carry eggs). Regarding females, morphometric maturity occurred at a carapace length (CL) of 11.50 mm, considering abdomen width as a reproductive character. Gonad maturity of females could be observed at a minimum size ranging from 15 to 17 mm CL. The smallest ovigerous female observed in the field was 15.60 mm CL, although a relevant population incidence of ovigerous females (86.6%) has just been observed at values higher than 17 mm CL. As for males, the relative growth of the left chela length changed at a value of 15.40 mm CL, while morphological changes in sexual tube occurred between CL of 14 and 16 mm. Testicular maturation occurred at a CL ranging from 17 to 19 mm. The smallest size of males having spermatozoids in their vasa deferentia was 18.70 mm CL. The results obtained indicated that, in both sexes, functional maturity occurred after morphometric maturity and at a size similar to that of gonad maturity. Comparing sexes, females acquired sexual maturity (morphometric, gonad and functional maturity) at sizes statistically smaller than those of males.     

Reproduction and sexual dimorphism in the viviparous lizard Sceloporus palaciosi (Squamata: Phrynosomatidae) from the Trans‐Mexican Volcanic Belt,Mexico

In this study, sexual dimorphism, reproductive cycles, litter size and offspring size of a population of the little‐known species Sceloporus palaciosi in central Mexico were analysed. Significant male‐biased sexual size dimorphism was recorded in snout–vent length (SVL), head length, head width, forearm length and tibia length. Both sexes showed asynchronous reproductive cycles, and males reached sexual maturity at a smaller SVL (33 mm) than females (37 mm). Testes volumes were small from January to February, testicular recrudescence began from March to June, and decreased in July, but increased again in August and September, followed by a second decrease from October to December. In females, vitellogenesis began from May until ovulation in December. Embryonic development extended from November to March, and a small number of females carried embryos through July. Mean litter size was 4.0 and was positively correlated with female SVL. The length of the reproductive period in S. palaciosi recorded in this study is longer than that recorded for other populations in other parts of this species range. Further studies are needed to clarify reproductive cycles in the other isolated populations of S. palaciosi, and then extended to other species and chromosome races in the Sceloporus grammicus complex.     

An atypical reproductive cycle in a common viviparous Asia Agamid Phrynocephalus vlangalii

Viviparous lizards living in cold climate of high altitude often exhibit atypical reproductive cycles, in which mating and fertilization occur synchronously and annually with parturition occurring at the end of the year. Nevertheless, detailed case studies on atypical reproductive cycles are few. Using anatomical data combined with behavioral observations, we examined the reproductive cycle of a common Asian agamid, Phrynocephalus vlangalii, from a high‐elevation area in Sichuan, China. Male spermiation of P. vlangalii occurred in May, and spermatogenesis began in June and reached a maximum in October. For females, ovulation and fertilization occurred in May, and females developed gestation and pregnancy in 3 months from June to August, without vitellogenesis during this period. Females gave birth synchronously in late August, then vitellogenesis began and lasted until May of the next year. All adult males and females were synchronized in the same reproductive condition each month. The synchronous and annual reproductive cycle of P. vlangalii clearly represents an atypical cycle. The male courtship and mating behaviors were concordant with gonadal cycle and mainly happened in May and June. Despite the short growth period for neonates, they had a high over‐winter survival rate of 84.4%, suggesting that autumn parturition did not generate high costs to this reproductive cycle. We propose that the high over‐winter survival rate of neonates is likely linked with female delayed sexual maturity, female asynchronous vitellogenesis and gestation, large relative clutch mass (RCM), and adult‐offspring burrow sharing behavior during hibernation.