Fishery sustainability depends on the long-term reproductive viability of a population, and this is an important element of fisheries management policies to maintain the resilience of populations . Thus, regular monitoring is necessary to detect changes in the reproductive potential of each stock.
Tuck et al.  suggested that adverse environmental conditions or a deprivation of sexual hormones may be responsible for female N. norvegicus resorbing their ovaries. Intensive fishing activity does not only affect populations directly but can also dramatically alter the environment. Bailey  found higher levels of ovary resorption in highly exploited populations of N. norvegicus when comparing them to less exploited populations. Possible explanations could be found in reduced oxygen levels, seabed disturbance and seismic or acoustic stress caused by human activity, especially trawling. Intensive lobster fisheries are also known to cause skewed sex-ratios if exploitation is sex-biased . Depending on the season and the gear, commercial catches of N. norvegicus often have a strong male-bias . The main reason for this is in the different burrow emergence behaviour of the two sexes due to reproductive constraints . In UK waters, ovigerous females are incubating eggs from summer for 8–10 months over winter until larvae hatch in the following spring . During incubation, female lobsters remain in their burrow for long periods of time and are, thus, less catchable than males, which emerge from their burrows more frequently and are therefore over-represented in the catches . Several studies have reported seasonal differences in the sex-ratios of N. norvegicus in trawl catches with a male bias, especially during the winter months [12, 21].
One common assumption is that the number of females is more important for the reproductive potential of a population than the number of males, as the production of female eggs involves higher metabolic costs than the production of male sperm . Females also produce eggs in much lower numbers than males produce spermatozoa, which are sometimes regarded as an inexhaustible resource. However, several studies on decapod crustacean species using experiments in holding tanks have actually shown that sperm supply can become a limiting factor for the reproductive success of a population (e.g. Pseudocarcinus gigas ; Callinectes sapidus ; Hapalogaster dentata ; Chionoecetes opilio ; Metacarcinus edwardsii . Sperm availability in a population depends on several factors, e.g. post-mating sperm regeneration intervals in the male, sperm storage capacity in the female and the longevity of spermatozoa. The operational sex ratio is another important factor, as well as male and female size distributions if mating is size assortative as in several other decapod crustaceans [28, 29]. The idea that ovary resorption in N. norvegicus may be due to a lack of insemination has been brought forward by several authors [4, 10]. De Figueiredo  studied the frequency of resorption in two populations of N. norvegicus off the Atlantic coast of Portugal (Alentejo and Algarve). She did not find a correlation between the percentage of females with resorbing ovaries and the incidence of females with empty spermatheca. However, this earlier study did not examine whether individual females with resorbing ovaries were inseminated. Our study therefore presents the first direct test of whether females of N. norvegicus with resorbing ovaries are actually inseminated. Our results show that a lack of insemination is not the cause for ovary resorption in N. norvegicus; all mature females studied herein carried spermatophores in their spermathecae and, thus, had mated.
Mating and sperm storage
Copulation in N. norvegicus is initiated by a brief courtship, followed by the transfer of ejaculate by the male gonopods which takes a few seconds only (CB pers. obs.). Sperm is assumed to be shed with the cuticle of the spermatheca when moulting. Thus, moulting and mating are closely linked and females need to re-mate each ovarian cycle. Herein, we present the first direct evidence of the loss of stored sperm during ecdysis, which is apparent in the complete shedding of the cuticle of the spermatheca. Our study of a pre-moult female shortly before ecdysis shows that male seminal secretions functioning as a sealant and spermatophores are already degraded at this stage. Whether this is due to the forthcoming moult or a consequence of the last process of fertilization remains unknown. The actual process of fertilisation, i.e. how stored sperm is released from the spermatheca and where exactly oocytes become fertilised, as well the histology of the spermatheca at this stage, has not been studied in N. norvegicus. However, in H. americanus, the process of fertilization has been confirmed to happen externally . Despite previous speculation that N. norvegicus may have internal fertilization , our data clearly suggests that the process of fertilization is external and probably very similar to H. americanus. In the latter species, the anterior suture is interpreted as the spermathecal orifice through which spermatophores enter the spermatheca during copulation while the two posterior sutures allow the spermatozoa to leave the spermatheca at the time of fertilization.
The morphology of the male internal reproductive organs of N. norvegicus has been studied previously , revealing a muscular sphincter between the middle and distal vas deferens which functions in portioning the sperm cord and its matrix into individual spermatophores. This sphincter may play an important role if males adjust the size and/or number of spermatophores they transfer during copulation. However, data on how many spermatophores are transferred to one female during copulation, is absent from the literature. Spermatophores are transferred together with vast amounts of seminal fluids, which harden and form a kind of sealant that occupies most of the space in the spermatheca. Such sealants are often interpreted as a mean to protect the male investment and may play an important role in sperm competition . Several individual spermatophores embedded in distinct portions of sealants were apparent in most of the studied spermathecae of N. norvegicus. Such a layering of male ejaculates in female sperm storage organs indicates their origin from different males and, thus, suggests that females copulate with consecutive mates within one reproductive season .
Promiscuity in female N. norvegicus is also evident through paternity testing. Multiple paternity was observed in more than 50% of female clutches in a population off the Portuguese Atlantic coast. Two to three males contributed approximately evenly in the fertilization of ova . Multiple paternity was also demonstrated in H. americanus  while broods of H. gammarus were found to be single-sired . Multi-paternity in H. americanus seems to be related to fishing intensity. At the Atlantic coast off Canada, multi-sired broods were observed in highly exploited populations while females from unexploited populations had single-sired broods . Sperm limitation might therefore not necessarily lead to a lack of insemination in females per se, but increase the number of matings in females as the amount (or quality) of sperm decreases. Future studies may target this issue by studying the operational sex ratios and the degree of multiple paternity in N. norvegicus broods to reveal whether exploited populations show indication of sperm limitation.
The incidence of ovary resorption and its seasonal dynamics
The frequency of full ovary resorption (stage 5b) is highest once the spawning season passes in autumn, and stays high throughout winter until it ceases in spring. This seasonality was evident in data from the Farn Deeps in the North Sea and agrees with the pattern observed in populations off the Portuguese Atlantic coast . The seasonal pattern of full ovary resorption may also explain the low levels of resorption observed in the western Irish Sea where most samples were taken in spring and summer. The highest proportion of resorbing females at 25% was observed in the additional samples from the Farn Deeps region where stages were assessed using a revised staging scale based on the incorporation of macroscopic and microscopic observations : bright yellow ovaries showed signs of resorption microscopically and represent a very progressed stage of resorption after all the green yolk is already reabsorbed (stage 1b). Those ovaries had not been recognised as a separate stage in the maturity scales adopted by AFBI and CEFAS. The actual proportion of females undergoing resorption may therefore be higher than the incidence detectable in their data. De Figueiredo  found even higher frequencies of resorbing ovaries (> 80%) in N. norvegicus populations off the Atlantic coast of Portugal.
Assuming an annual reproductive cycle, the majority of mature females should carry eggs in the season where incubation takes place (summer to spring in the following year). The natural proportion of berried females cannot be drawn from collected data as berried females are believed to remain in their burrows most of the time, and thus, are under-represented in catches . Nevertheless, the high incidence of large (mature) females, without clutches, in samples from the North Sea during the incubation period, may indicate that in this area there is an increased prevalence of females that had undergone resorption previously and already re-entered the regular ovary maturation cycle.
Ovary resorption and female body size
If full ovary resorption was more frequent in smaller females, one could hypothesize that it mainly occurs in females that start maturing for the first time. The first onset of sexual maturity does not seem to occur at a specific season of the year . As a result, the first reproductive cycle of young females is not in synchrony with the regular seasonal reproductive cycle of other (older) sexually mature females. The first maturation of the ovary may therefore not lead to a successful spawning but could be regarded as a test run which may also lead to full ovary resorption if ovary maturation is not completed until spawning season. However, this is not supported by our data. According to the interpretation of Bailey  that full ovary resorption is a “reset the clock”-strategy of larger (older) females, the occurrence of resorption should be positively correlated with body size. This was supported by data on N. norvegicus [10, 36] collected off the west coast of Scotland (Sound of Jura and Firth of Clyde). The study in the Firth of Clyde further supported Bailey’s hypothesis as the length frequency curves developed in his study indicate that the reproductive cycle may take longer than a year . However, a negative correlation was found between ovary resorption and body size off the West coast off Portugal . Our analysis support Bailey’s hypothesis only with regard to females from the Farn Deeps region in the North Sea—where resorption was high—but not in females from the western Irish Sea. The latter populations show in general smaller body sizes than specimens from the North Sea (see Additional file 3: Fig. S2). This may not only explain that body size did not show a positive correlation with the frequency of ovary resorption, but also be responsible for the total proportion of resorption being very low (< 1%) in the western Irish Sea populations. Furthermore, the timing of the surveys conducted in the western Irish Sea (summer) was unsuitable to assess the degree of full ovary resorption as the highest frequency is expected later in the year, once the spawning season has passed in autumn.
As in many decapod crustaceans, the reproduction, or at least the reproductive cycle of females, is linked with the moult cycle. Females moult after larvae have hatched from the clutch and mate immediately afterwards, while their exoskeleton is still soft (“soft-shelled mating” ). Many decapods show this type of moulting and mating link [11, 37]. However, copulation can also occur in intermoult females (“hard-shelled mating” ) and some decapod species show both pathways (e.g. ). Another important factor with regard to the timing of the female moult is the period of incubation. The clutch of eggs attached to female pleopods, would be lost when the exoskeleton is shed at ecdysis. As incubation takes approximately up to 9 months in western Irish Sea and North Sea N. norvegicus populations, moulting of berried females can only occur within the short time frame between hatching and spawning of the next generation. Based on the morphology of the spermatheca in a pre-moult female, it seems likely that the discharging of the spermathecal content is necessary to receive and store fresh spermatophores for the next reproductive cycle. Thus, moulting must occur at a set point of time in reproductively active females. Males are known to be more flexible about the timing of ecdysis and moult more frequently than females . As a consequence, males grow faster and are on average larger than females of the same (supposed) age . Resorbing their ovaries and skipping a reproductive cycle from time to time may allow females more flexibility in terms of moulting and, thus growth. This leads us to the question whether females actually resorb because they are larger or if females are larger because they resorb.