Male Spermatophores Research Articles

A complex sexual cycle in sandy beaches: the reproductive strategy of Emerita brasiliensis (Decapoda: Anomura)

Reproductive tactics displayed by the mole crab Emerita brasiliensis that inhabits Atlantic beaches of South America are reported. The analysis of external sexual characters and reproductive organs disclosed seven developmental forms: megalopae, neotenic males, early females, juveniles, males, females (ovigerous or not) and intersex individuals. Precocious acquisition of gonopores in females, production of spermatophores in neotenic males and presence of juveniles and intersex individuals are reported for the first time for this species. Sex ratios were biased towards male forms in summer, whereas the opposite trend was observed in autumn. The occurrence of different forms within a single population, coupled with a marked temporal variability in its abundance, suggest a high complexity in the sexual life cycle of the mole crab. This involves two different pathways: (a) short, where megalopae moult into neotenic (mature) males or early females; and (b) long, following a sequence of moults involving several stages (zoeas, megalopae, juveniles and adults).

Reproductive Behavior of the Japanese Spineless Cuttlefish Sepiella japonica

The reproductive behavior of the Japanese spineless cuttlefish Sepiella japonica was observed in a tank. The males competed for females before egg-laying and then formed pairs with females. The male then initiated mating by pouncing on the female head, and maintained the male superior head-to-head position during the mating. Before ejaculation, the male moved his right (non-hectocotylized) arm IV under the ventral portion of the female buccal membrane, resulting in the dropping of parts of spermatangia placed there during previous matings. After the sperm removal behavior, the male held spermatophores ejected through his funnel with the base of hectocotylized left arm IV and transferred them to the female buccal area. The spermatophore transfer occurred only once during each mating. The female laid an egg capsule at average intervals of 1.5 min and produced from 36 to more than 408 egg capsules in succession during a single egg-laying bout. Our results also suggested one female produced nearly 200 fertilized eggs without additional mating, implying that the female have potential capacity to store and use active sperm properly. The male continued to guard the spawning female after mating (range=41.8-430.1 min), and repeated matings occurred at an average interval of 70.8 min during the mate guarding. Although the time spent on the sperm removal in S. japonica was shorter than in other sperm-removing cuttlefishes, the shorter sperm removal duration may be compensated by the post-copulatory mate guarding and repeated matings in this species.

Description of the male reproductive apparatus of the hermit crab <i>Calcinus tubularis</i> (Decapoda: Anomura: Diogenidae)

We describe for the first time the male reproductive apparatus, spermatophore and sperm of Calcinus tubularis, analysing them under interference phase microscopy, scanning electron microscopy and transmission electron microscopy. The testes merge into a tubular duct made up of four zones. In the proximal zone, the ampulla of the spermatophore starts to be formed. In the medial zone, the ampulla is completed, the stalk lengthens and the foot develops. The two halves making up the ampulla meet at the lateral ridge, which shows a mostly fibrillar ultrastructure. Spermatozoa are composed of an almost spherical acrosomal vesicle, capped by a conical operculum, a cytoplasm, a nucleus and three microtubular arms. The acrosomal vesicle is posteriorly penetrated by the perforatorial chamber and shows an inner acrosome zone, a thick ray zone and an electron dense outer acrosomal zone. The great importance of paguroid male reproductive apparatus morphology and ultrastructure for phylogenetic analysis is confirmed.

Male field crickets that provide reproductive benefits to females incur higher costs

Abstract. 1. Females often select mates based on signals correlated with the quality of the direct benefits that males will provide to them. A male's quality as a mate and the structure of his mating signals may covary because both traits are energetically expensive for males to produce and because both traits are affected by short‐term changes in nutritional condition.2. In the variable field cricket, Gryllus lineaticeps, previous work has shown that females receive reproductive benefits from males that produce higher chirp rates and lifespan benefits from males that produce longer chirp durations, even when they only receive the sperm and seminal fluid contained in male spermatophores. Higher chirp rates are energetically expensive for males to produce, and chirp rate is strongly affected by diet quality, whereas longer chirp durations do not appear to be expensive for males to produce, and chirp duration does not appear to be affected by male diet quality. In this study two hypotheses were tested about the energetic costs of spermatophore production: (1) that spermatophores are expensive for males to produce and (2) that males providing greater direct benefits to females incur higher costs of spermatophore production.3. Males that were provided with a lower quality diet took longer to produce a new spermatophore. This result suggests that spermatophores are costly for males to produce.4. Males that produced higher chirp rates took longer to produce a new spermatophore. This result suggests that male chirp rate and female reproductive benefits may covary because both traits are energetically expensive for males to produce and thus are affected by male nutritional condition. There was no association, however, between male chirp duration and spermatophore production time.

Hybridization between the freshwater prawns Macrobrachium rosenbergii (De Man) and M. carcinus (L.)

The production of hybrids between Macrobrachium rosenbergii and other Macrobrachium species has great economical importance for aquaculture, but also has serious environmental implications when M. rosenbergii is present as an exotic species. In this study, intra- and interspecific crosses between M. rosenbergii and M. carcinus were carried out through natural mating and artificial insemination. For the natural crosses, a fertile female was placed inside an aquarium with a mature male and the behavior of animals was monitored. For the artificial insemination assays, male spermatophores were collected by electroejaculation and placed inside the sperm receptacle of a fertile female. The temperature was maintained at 27±2 °C during the study. Firstly, 62 and 45 natural intraspecific crosses were carried out in M. rosenbergii and M. carcinus, with larvae obtained from 32.3% and 57.8% of the crosses, respectively. Thirty-seven natural interspecific reciprocal crosses were also attempted but no mating occurred. A total of 57 and 39 intraspecific crosses were carried out by artificial insemination in M. rosenbergii and M. carcinus, obtaining larva from 22.8% and 41.0% of the crosses, respectively. Finally, 46 interspecific reciprocal crosses were also carried out by artificial insemination. Hybrid zygotes were produced in all the crosses, but embryo development did not progress further than the gastrula stage. This indicates the existence of both behavioral and postzygotic reproductive isolation barriers. These barriers could prevent the hybridization of these species in the natural environment.

BEHAVIOR OF JUVENILES OF THE JAPANESE ENDEMIC SPECIES CAMBAROIDES JAPONICUS (DECAPODA: ASTACIDEA: CAMBARIDAE), WITH OBSERVATIONS ON THE POSITION OF THE SPERMATOPHORE ATTACHMENT ON ADULT FEMALES

Abstract The behavior of juveniles of the Japanese endemic crayfish Cambaroides japonicus (Decapoda: Cambaridae) was observed in the field and in the laboratory. In addition, the occurrence and placement of spermatophores on adult females is described from specimens inhabiting small brooks at Otaru and Hamamasu, Hokkaido, Japan, sampled from 1998 to 1999. The second stage juveniles left their mother permanently after some exploration behavior. In adult females, spermatophores were attached to the surface of the seminal receptacle (annulus ventralis), which is situated at the posterior margin of the seventh thoracic sternite. In C. japonicus the invagination of the annulus ventralis is not deep enough to hide the male spermatophores. Previous studies of the Astacidae reported that juveniles left their mother at the second stage, that spermatophores were attached to the surfaces of sternal plates of the last three pereopods, and that an annulus ventralis did not exist. In contrast, Cambaridae juveniles norm...

Fitness advantage from nuptial gifts in female fireflies

Abstract 1. In many insects, males provide nuptial gifts to females in the form of spermatophores, sperm‐containing structures produced by male accessory glands.2. The work reported here examined the influence of both spermatophore number and spermatophore size on female reproductive output in two related firefly beetles, Photinus ignitus and Ellychnia corrusca (Coleoptera: Lampyridae). Based on differences in adult diet, male spermatophores were predicted to increase female reproductive output to a greater extent in P. ignitus than in E. corrusca.3. Female fecundity was significantly higher in triply mated females than in singly mated females in both species, with no difference between mating treatments in female lifespan or egg hatching success. No effects of second male spermatophore size on fecundity, lifespan, or egg hatching success were detected in either species.4. These results suggest a direct fitness advantage from multiple mating for females in both species, although enhanced fecundity may be due either to allocation of spermatophore nutrients to eggs or to other substances transferred within the spermatophore acting as oviposition stimulants.

Vertical transmission of gill-associated virus (GAV) in the black tiger prawn Penaeus monodon.

Chronic gill-associated virus (GAV) infection is endemic in Penaeus monodon broodstock captured from north-east Queensland in Australia and in farmed shrimp produced from these. We investigated the role of vertical transmission in perpetuating the high prevalence of these chronic GAV infections. Reverse transcription (RT)-nested PCR detected GAV in spermatophores and mature ovarian tissue from broodstock and in fertilized eggs and nauplii spawned from wild-fertilized females. In laboratory-reared P. monodon (> 12 mo old) that had a high mortality rate, RT-nested PCR detected GAV in male spermatophores at levels significantly higher than that detected in the lymphoid organ. By transmission electron microscopy (TEM), GAV virions were detected in spermatophore seminal fluid, but not sperm cells. Histological evidence of hypertrophied cell foci (spheroids) and TEM observation of GAV nucleocapsids and virions in spheroid cells was also found in 100% of lymphoid organs of approximately 1.2 g juvenile P. monodon reared in the laboratory from postlarvae collected from commercial hatcheries. Sequence analysis of PCR amplicons from parental P. monodon and fertilized eggs of artificially inseminated broodstock indicated that GAV associated with eggs can originate from both the male and female parents. Although the female GAV genotype was predominant in eggs, there was some dependence on infection levels in the male and female shrimp as indicated by RT-PCR. RT-nested PCR data on GAV levels in eggs, nauplii, protozoea and PL5 progeny of the artificial matings suggests that vertically transmitted virus is most probably associated with the egg surface.

Distant lovers: spermatophore deposition and destruction behavior by male springtails.

Males of the springtail Orchesella cincta transfer their sperm indirectly using spermatophores. The present study aimed to investigate how individual males maximize their reproductive success. In an experiment examining the role of chemical communication, it appeared that the males deposit their spermatophores preferentially on patches which have been conditioned with conspecifics. Varying conditioning intensity resulted in a response which can be described by a saturation curve. In a comparison involving a related species the conditioning effect was strictly species specific. An experiment where the sexes were compared showed that conditioning with males exerts a slightly stronger effect than conditioning with females. In another experiment spermatophore depositing males showed a strong preference for patches with spermatophores of previous males, which they replaced with their own. An explanation for this may be that the males parasitize each other's scent marks. When a number of males are kept together they destroy most of each other's spermatophores. The destruction behavior is specifically displayed by males in their reproductive phase. Video recordings showed that deliberate destruction of spermatophores takes place by eating them and that the males are able to recognize and spare their own spermatophores.

The potential for incorporation of male derived proteins into developing eggs in the leafhopper Bothrogonia ferruginea

The leafhoppers, Bothrogonia ferruginea (Homoptera: Cicadellidae), eclose to adults in summer with immature reproductive organs. The adults live for 10 months including a hibernation of 4 months. Overwintered females mate multiply in spring. Eggs develop rapidly and are laid continuously in this mating period. Males produce sperm-bundles in which sperm are attached in a row to a rope-like hyaline material, and transfer them to the female via a large spermatophore that is placed in her bursa copulatrix. After mating, sperm are separated and removed to a spermatheca for storage prior to fertilization, but the sperm-binding material (trypsin degradable proteins) and the spermatophore disappear in the bursa and an enlarged portion of the genital duct. An injection of rhodamine B-dyed proteins into the female bursa with a microsyringe results in the production of intensely fluorescent eggs developing in the ovaries. This suggests that females could incorporate proteinaceous material derived from male spermatophores and/or sperm-binding material into their oocytes.

Fate of Male-derived Cucurbitacins in Spotted Cucumber Beetle Females

Using the spotted cucumber beetle, Diabrotica undecimpunctata howardi, as a model species, we begin an examination of the role of dietary cucurbitacins, the bitter tetracyclic triterpenes produced by cucurbits, in the reproductive behavior of luperine chrysomelids that seek these compounds for purposes other than host-plant recognition or nutrition. By manipulating the cucurbitacin content of adult diets, we determine: (1) how males and females partition cucurbitacins between reproductive organs and other tissues, (2) the extent to which males pass cucurbitacins to females during copulation, and (3) if females increase their cucurbitacin stores via multiple matings. After two days of exposure to dietary cucurbitacins, 8.3 times more cucurbitacins per gram dry weight were sequestered in male spermatophores than in the aggregate of remaining male tissues. These cucurbitacin-rich spermatophores were passed to females during mating, and 78.8% of the transferred cucurbitacin was deposited in eggs, 11.8% was irreversibly sequestered in other female tissues, and 9.4% was apparently excreted. Females copulated with 0–15 males prior to accepting a complete spermatophere, but did not accept measurable amounts of cucurbitacin from rejected males. Regardless of when it was received, females lost subsequent receptivity to additional males after accepting a complete spermatophore. The implications of these data are discussed in terms of sexual selection hypotheses and mating behavior in cucumber beetles.

Objective assessment of maturity in the Patagonian squid Loligo gahi (Cephalopoda: Loliginidae) from Falkland Islands waters

An objective assessment of maturity in the loliginid squid Loligo gahi was tested using a method developed for L. pealeii utilizing principal component and discriminant analyses. Samples were taken from both seasons of the commercial fishery in the Falkland Islands (prosecuted south of 51°20′S) in 1994 and 1995. In addition, research samples were taken in January, June, and November, outside the fishing seasons, to provide individuals of a greater range of size and maturity. The method, using a combination of indices of somatic and gonad lengths and scoring abundance of eggs and spermatophores in females and males, respectively, proved to be successful both in a research context, when variables can be measured to a high degree of precision, and in a fisheries context where less precision is practicable. The method also detected anomalies in the maturity status of squid that might have been overlooked in a more subjective assessment, corroborating the accumulating evidence for batch-spawning in loliginid squid. Four stages of maturity were recognized for female squid and three for male squid.

Differential allocation of male-derived nutrients in two lampyrid beetles with contrasting life-history characteristics

Across diverse animal taxa, sperm is transferred from males to females during mating within a spermatophore produced by male accessory glands. In some insects, male spermatophores provide females with nutrients that may be used to increase reproductive output or for somatic maintenance, while in others no such benefits have been detected. Boggs suggested that variation in the current function of spermatophores may be explained by considering ecological and life-history factors. This study examined spermatophore function in Ellychnia corrusca and Photinus ignitus (Coleoptera: Lampyridae), two beetles that exhibit marked differences in adult diet, adult life span, and overwintering stage. During mating, males of both species transfer to females a complex, proteinaceous spermatophore, which is subsequently digested in a specialized sac within the female reproductive tract. Males of each species were injected with 3 H‐radiolabeled amino acid mixtures and mated with conspecific females. The fate of spermatophore-derived proteins was determined by dissecting females at various times after mating with these radiolabeled males. Females of these two species showed markedly different patterns of incorporation of spermatophorederived nutrients. P. ignitus females incorporated the majority (62%) of spermatophore-derived protein into maturing oocytes within 2 days after mating. In contrast, in E. corrusca a large percentage of radiolabel (46%) appeared in female fat body at 6 days after mating, with a threefold lower allocation to maturing oocytes compared to P. ignitus. These findings support the prediction that short-lived, nonfeeding females are selected to allocate a greater proportion of male-derived nutrients to reproduction, while longer-lived, feeding females are selected to allocate a greater proportion to somatic reserves and maintenance. These results suggest that life-history characteristics may be useful in explaining observed differences in spermatophore function across taxa. Key words: Ellychnia, firefly, life history, nuptial gifts, paternal investment, Photinus, radiotracer, spermatophore. [Behav Ecol 10:97‐104 (1999)]

Delayed mating and its cost to female reproduction in the butterfly,Eurema hecabe

The timing of mating of females under semi-natural condition, male ejaculate production and their effects on female fecundity were examined inEurema hecabe. Age of the first mating of females varied, and the number of matings increased with age. Male spermatophore production depended on age and body mass. The spermatophore mass at the second mating depended only on the interval between the first and second matings. The timing of the first mating and the spermatophore mass did not affect female fecundity. The timing of mating of females relative to the role of male spermatophores in female fecundity and male mating strategy are discussed.

The formation, transfer, and fate of spermatophores in Photinus fireflies (Coleoptera: Lampyridae)

Fireflies in the genus Photinus have been assumed previously to be among the many insect species in which males transfer primarily sperm during mating. In this study, male P. ignitus and P. marginellus were found to produce a complex proteinaceous spermatophore in four paired male accessory glands, a major component of the spermatophore being formed within prominent spiral glands. The spermatophore is transferred to the female within the first 40 min of copulation, and sperm bundles are released into the spermatheca. The remainder of the spermatophore subsequently undergoes digestion within a specialized sac in the female reproductive tract. To examine the function of male spermatophores, male P. marginellus were fed rhodamine B, resulting in the production of intensely fluorescent spermatophores. After mating with rhodamine-dyed males, females incorporated material derived from male spermatophores into their oocytes within 58 h post mating. Nutrient donations from males during mating are expected to play particularly important roles in female oogenesis in insects with nonfeeding adults, such as Photinus spp. The presence of spermatophores in Photinus is related to marked differences among species in their life histories, mating systems, and mating behaviors.

Cryptic female choice predicated on wing dimorphism in decorated crickets

Male decorated crickets, Gryttodes sigllatus, normally lack bind wings and are incapable of flight (short-winged males), but occasionally exhibit fully developed hind wings that make rudimentary flight possible (long-winged males). Long-winged males bear a cost of flight in the form of decreased insemination success, which arises as a consequence of two interrelated factors: (1) long-winged males exhibit a lower reproductive investment relative to short-winged males, as measured by the mass of a male's spermatophore and reproductive organs and (2) the postcopulatory behavior of females favors males that maximize their reproductive investment. Of particular importance to male mating success is the spermatophylax, a large gelatinous mass forming part of the spermatophore and consumed by the female after mating. Consumption of the spermatophylax keeps the female preoccupied while sperm are discharged from the remaining portion of the spermatophore (sperm ampulla) into her repro ductive tract. The spermatophylax of long-winged males is significantly smaller than that of short-winged males and consequently requires less time to consume. As a result, the sperm ampulla of long-winged males is frequently removed before its complete evacuation and significantly sooner than that of short-winged males. Because the spermatophore-removal behavior of females mediates the relative insemination success of short-winged and long-winged males, it can be considered a form of cryptic female choice

Protein content of spermatophores in relation to monandry/polyandry in butterflies

The evolution of a mating system, and specifically mating frequency, is dependent on the costs and benefits to both sexes of mating once or several times. In butterflies, males transfer a spermatophore that contains both sperm and accessory gland products. Accessory gland substances contain nutrients which, in some species, females use to increase their reproductive output and longevity. Nutrients contained in these packaged ejaculates represent investment by males in reproduction. Consequently, the nutritional composition of spermatophores may vary depending on the mating system. There are two lines of arguments concerning the evolution of the nutrient content of ejaculates. One hypothesis argues that male nuptial gifts evolved in the context of certainty of paternity and ease of finding mates; thus spermatophores of polyandrous males (with lower certainty of paternity and greater ease of finding mates) should contain less protein than those of monandrous males, since more spermatophores are produced on average. The other hypothesis argues that polyandry evolved in the context of maximization of male transfer of nutrients to females, and hence spermatophores of polyandrous males should contain more protein than those of monandrous males. In an attempt to distinguish between these two hypotheses, we determined how protein content of ejaculates varied with the degree of polyandry in nine species of pierid and two species of satyrid butterflies. We found that both relative ejaculate mass and protein content increased with the degree of polyandry. Hence our results are consistent with the view that polyandry has evolved in the context of male transfer of nutrients to females, and provides another example of a male adaptation to multiple mating in butterflies.

京都府沿岸域に来遊するアオリイカの産卵生態について

From diving observations and spawning examination using artificial substrata settled on the sea bed at 5-50m depths in the sea off Kyoto prefecture, the spawning season and spawning grounds of the oval squid Sepioteuthis lessoniana were studied from April to July, 1991. With a rise in water temperature above 16°C in coastal waters, mature females migrated to the inshore spawning grounds in the middle of May to lay their eggs. The depth of spawnIng gradually descended during the spawning period to the 30-40m depth range in the middle of June. Samples of mature males and females were collected off Kyoto prefecture using set nets from May to July, 1991. All investigated females, including those without spermatophores embedded in the buccal membrane, had sperm in their seminal receptacles. The average number of spermatophores of males decreased during the spawning period. Judging from the maximum number of spermatophores of a male that embedded in the buccal membrane of a female, males may copulate repeatedly about 10 times during the spawning period.

Spernathecal morphology, sperm transfer and a novel mechanism of sperm displacement in the rove beetle, Aleochara curtula (Coleoptera, Staphylinidae)

The mechanism by which sperm are transferred from the male's spermatophore to the female's storing cage is described for the rove beetle Aleochara curtula, emphasizing a novel mechanism of sperm displacement by competing males. The cuticular, U-shaped spermatheca is equipped with a valve structure and two sclerotized teeth. The tube of the spermatophore extends into the spermathecal duct through the guidance of the flagellum of the male endophallus. Further elongation of the spermatophore tube, however, occurs only after separation of the pair. A primary tube bursts at its tip after passing through the valve. Within the lumen of the primary tube, a second tube passes through the valve and continues to extend up to the apical bulb of the spermatheca, doubles back on itself and swells to form a balloon filling most of the spermatheca. The balloon of the spermatophore is pierced within the spermatheca by tooth-like structures pressed against the spermatophore through contraction of the spermathecal muscle. The same process of spermatophore growing and swelling is also observed in mated females. Sperm from previous copulations are backflushed through the valve and the spermathecal duct, indicative of last-male sperm predominance.

Neural and hormonal regulation of calling behavior in Blattella germanica females

Virgin females of the German cockroach, Blattella germanica, exhibit cycles of calling behavior in relation to the cycles of corpora allata activity and ootheca production. The roles of juvenile hormone, mating, and the ootheca in the regulation of calling behavior were investigated. The onset of calling in relation to increasing rates of juvenile hormone synthesis suggested involvement of the corpora allata. Allatectomy prevented the expression of calling behavior and treatment with the juvenile hormone analog fenoxycarb restored calling. Corpus allatum denervation through nervi corporis allati transection, which accelerates the synthesis of juvenile hormone by the corpora allata, also accelerated the onset of calling. Using castrated males, timed interruption of mating and ventral nerve cord transection, we demonstrated that, while insertion of the male genitalia and/or spermatophore in the bursa copulatrix caused an immediate suppression of calling behavior, presence of sperm and/or associated seminal fluid in the spermatheca was required for the complete inhibition of calling in the first as well as in the second ovarian cycle. Although inhibitory signals from the presence of an ootheca in the genital atrium would suppress calling behavior indirectly by inhibiting corpus allatum activity, treatment of gravid females with fenoxycarb suggested that signals from the ootheca also inhibit calling directly. The ventral nerve cord plays a critical role in the transmission of inhibitory signals from mating and from the presence of the ootheca.