Male Isaza (Gymnogobius isaza, Gobiidae) prefer large mates: a counterstrategy against brood parasitism by conspecific females

Like many other gobies, male Isaza (Gymnogobius isaza) which are endemic to Lake Biwa, Japan, exclusively care for broods in nests. This goby may have an optimal range of brood size (i.e., an average clutch size of about 2000–3000 eggs) within which they may produce larger numbers of hatching young because much larger broods may be destroyed by fungal infection before hatching. This optimal brood size hypothesis (Takahashi et al. in J Ethol 22:153–159, 2004) predicts that (1) after spawning, both males and females will refuse additional spawning by other gravid females (second females) to keep brood sizes within optimal ranges, (2) larger fish will repel second females more successfully than will smaller fish, and thus, (3) both sexes prefer larger mates. To examine these predictions, we first observed Isaza’s aggressive behaviors in aquaria and investigated whether fish attacked and repelled second females that were introduced after spawning, and, if so, what were the sizes of fish that did so. Large fish, regardless of sex, aggressively prevented second females from entering the nest, but second females larger than the pairs displaced the pair females forcibly and spawned eggs into their clutches. Mate choice experiments showed that males preferred large females. Although females’ choice of large mates was not confirmed, many results may largely coincide with the predictions of the optimal brood size hypothesis. Thus, Isaza males’ choice of large mates will be advantageous for defending against brood parasitism by conspecific females and for achieving optimal clutch size.     

Simultaneous spawning by female stream goby Rhinogobius sp. and the association with brood cannibalism by nesting males

A laboratory experiment was conducted by varying the undersurface area of nesting substratum and the number of females in an experimental tank to elucidate the determinants of the mating pattern in the stream goby, Rhinogobius sp. cross‐band type. Males with larger nests tended to attract two or more females to their nest in a tank. Moreover, males spawned simultaneously with multiple females and entire brood cannibalism by males was rarely observed under a female‐biased sex ratio. When males spawned with a single female with low fecundity, however, entire brood cannibalism occurred at a high frequency, suggesting that a male guarding a nest with fewer eggs consumes the brood. Therefore, spawning behaviour of females that leads to a large egg mass would decrease the risk of entire brood cannibalism. In this species, simultaneous spawning by multiple females in a nest serves as a female counter‐measure against entire brood cannibalism. These results suggest that a conflict of interest between the sexes through brood cannibalism is a major determinant of simultaneous spawning.     

Simultaneous polygyny of the gobiid fish Asterropteryx semipunctata in relation to mate availability

Nesting males of Asterropteryx semipunctata conducted spawning behavior with 2–6 females simultaneously. We carried out field observations on a rocky reef in Kagoshima, Japan, to examine the hypotheses that large males will show multi-female spawning behavior because of their mating advantage, and that simultaneous multi-female spawning will occur when the operational sex ratio (OSR; the ratio of receptive males to receptive females) becomes female-biased. Contrary to our prediction, neither the total number of multi-female spawnings during a spawning season nor mean number of spawning females at a time were correlated with nesting male sizes. This indicates that larger males often did not conduct multi-female spawnings. As predicted, the incidence of multi-female spawning followed the change in the OSR over time—as the OSR in the study area became biased toward females, the incidence of multi-female spawnings gradually increased. Our results suggest that mate availability affects mating patterns in A. semipunctata.     

Reproductive behaviour of the filefishRudarius ercodes: male spawning parades and female choice

Synopsis The reproductive behaviour ofRudarius ercodes is described from undersea observations in Aburatsubo Bay, Japan. Reproductive behaviour can be separated into four parts: (1) Prespawning Search = searching for spawning sites by females and searching for gravid females by males, (2) Spawning Parade = males follow a gravid female in a line, competing with each other to reach the head of the queue, (3) Spawning = the female takes the spawning position, males rush to the side of the female, and mating occurs between one female and several anterior males of the spawning parade, (4) Parental Care = females attach adhesive eggs to seaweed with the mouth and guard them until embryos hatch. There is no male parental care. The reproductive season ranges from May to October and spawning occurs early in the morning every day. Females begin feeding early in the morning, but males feed little at this time.R. ercodes shows neither territorial behaviour nor fixed-pair spawning. One male might spawn several times in one morning. One female spawns at most once every 5 days. The mating system of this species is promiscuous. The probable function of the spawning parade as a style allowing female choice is discussed.     

Intentional multiple mating by females in a species where sneak fertilization circumvents female choice for parental males

This paper describes how individual female ocellated wrasse Symphodus ocellatus distribute their spawning among males and nests in space and time. It is based on previously collected genetic data of larvae from ten different nests (used to reconstruct half and full‐sibling groupings both within and among nests on multiple days) and behavioural data of marked females across the reproductive season. Both the genetic analyses and behavioural observations confirm that female S. ocellatus intentionally engage in multiple mating, by repeatedly spawning at the same nest on different days and at several different nests (up to 12 spawning events over 3 weeks), leading to mixed paternity among her young. The main benefit of such high and intentional multiple mating is probably insurance against brood failure due to nest predation, desertion or poor paternal care by the male. These findings reveal that even in systems where females attempt to avoid male‐controlled mixed paternity, they may still engage in intentional multiple mating due to these potential benefits.     

Reproductive ecology of the jacky dragon (Amphibolurus muricatus): an agamid lizard with temperature‐dependent sex determination

Abstract The jacky dragon, Amphibolurus muricatus (White, ex Shaw 1790) is a medium sized agamid lizard from the southeast of Australia. Laboratory incubation trials show that this species possesses temperature‐dependent sex determination. Both high and low incubation temperatures produced all female offspring, while varying proportions of males hatched at intermediate temperatures. Females may lay several clutches containing from three to nine eggs during the spring and summer. We report the first field nest temperature recordings for a squamate reptile with temperature‐dependent sex determination. Hatchling sex is determined by nest temperatures that are due to the combination of daily and seasonal weather conditions, together with maternal nest site selection. Over the prolonged egg‐laying season, mean nest temperatures steadily increase. This suggests that hatchling sex is best predicted by the date of egg laying, and that sex ratios from field nests will vary over the course of the breeding season. Lizards hatching from eggs laid in the spring (October) experience a longer growing season and should reach a larger body size by the beginning of their first reproductive season, compared to lizards from eggs laid in late summer (February). Adult male A. muricatus attain a greater maximum body size and have relatively larger heads than females, possibly as a consequence of sexual selection due to male‐male competition for territories and mates. If reproductive success in males increases with larger body size, then early hatching males may obtain a greater fitness benefit as adults, compared to males that hatch in late summer. We hypothesize that early season nests should produce male‐biased sex ratios, and that this provides an adaptive explanation for temperature‐dependent sex determination in A. muricatus.     

Vagabond males and sedentary females: spatial ecology and mating system of the speckled rattlesnake (Crotalus mitchellii)

We used radiotelemetric data and behavioural observations to characterize seasonal (mating versus post‐mating seasons) and sexual variation in movement patterns, as well as to examine some of the ecological factors contributing to the evolution of the mating system in a venomous predator from the Mojave Desert of North America, the speckled rattlesnake, Crotalus mitchellii. Mating occurs in spring from late April to early June, shortly after emergence from hibernation, when snakes are predictably aggregated around the dens. Males and females travelled further per unit time in the mating season compared to the post‐mating season. Males also travelled longer distances per unit time than females in the mating and post‐mating seasons, and males with larger home ranges during the mating season had more potential mating partners. The results obtained suggest that males actively locate females during the mating season, and that the drastic increase in distance travelled by males during the mating season may be caused by strong male–male competition for access to females, probably because of the limited availability of sexually receptive females. Furthermore, males fight for access to females, and males of larger size are more likely to acquire females. Therefore, sexual selection apparently acts on two different male phenotypic traits: investment in mate‐searching activities and male body size. The present study demonstrates that combining quantitative spatial analyses and behavioural observations in an explicit temporal context can significantly advance our understanding of the ecology and evolution of organismal mating systems. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 681–695.     

Mate choice by males of the hermit crab Pagurus filholi: Do males assess ripeness and/or fecundity of females?

Males of the hermit crab, Pagurusfilholi, often grasp the edges of shells occupied by females and drag them during the mating season. This behavior was experimentally confirmed to be a precopulatory guarding behavior displayed by males for ripe females, and males were found to recognize females which were within about 5 days of spawning. Most theoretical models for mating preference assume the choosing sex (the male in the present case) has complete reproductive information about potential mates, and predict that males will preferably choose more fecund females and/or females that will require less guarding time (i.e. that will spawn sooner) as partners. Several male-choice experiments between two ripe females, both previously guarded by other males, were carried out to examine the above predictions. Males did not prefer females of larger size, higher fecundity or with less time remaining until spawning. These results suggest that males may not have complete information about potential partners, rather that male hermit crabs may adopt a mating strategy of pairing with the first ripe female they encounter. Even with such incomplete mate assessment, males may enhance their reproductive success by recognizing ripe females that will spawn within a given time (about 5 days in the present case).     

Sex-ratio,seasonality and long-term variation in maturation and spawning of the brown shrimp <Emphasis Type="Italic">Crangon crangon</Emphasis> (L.) in the German Bight (North Sea)

Aspects of the reproductive and maturation biology of the brown shrimp Crangon crangon (L.) were studied in various subareas of the German Bight (North Sea). The size-specific sex ratio of C. crangon was examined based on length frequency distribution data. The sex ratio for the smallest size groups at which sex was determined was typically around 0.5, indicating an even ratio between males and females. The proportion of females decreased in the 30–45 mm size range. In length classes larger than 50 mm, the proportion of females constantly increases to 100% at around 60 mm total length. We concluded that sex reversal from male to female may not occur in C. crangon. Size at sexual maturity was determined from the proportion of ovigerous females. Size at maturity (L ₅₀) was estimated as 55.4 and 62.0 mm total length for spring and winter data, respectively. The seasonal spawning cycle was studied over the period 1958–2005. Between mid February and late June and for size classes larger than 65 mm ovigerous shrimps exceeded 80% and reached up to 100% of the females in the population. This period can be seen as the core spawning season. From early August to early December the proportion of ovigerous shrimps in the female population is very low. Interannual differences in the seasonal process are obvious with a dramatic decline in C. crangon reproductive success in the late 1980s. Various options are discussed for the reasons of the decline and recovery of the reproductive performance.     

Spawning behaviour ofCheimerius nufar in captivity

Synopsis The santerCheimerius nufar is widespread in tropical and subtropical waters of the western Indian Ocean and forms an important component of linefish catches along the east coast of southern Africa. Observations of spawning behaviour in captivity have revealed that spawning occurs during spring over a period of four months. Mating takes place at sunrise and may continue for up to 105 min (mean duration = 60 min). During spawning males become dark with prominent white markings. They become very aggressive and set up territories. Females remain a uniform silvery-pink. Mating occurs between males and females of similar sizes, culminating in egg and sperm release near the surface. Individual fish spawned up to 14 times during a morning. Streaking occurred throughout the season, with a second male joining a spawning pair and releasing gametes simultaneously. Slinger,Chrysoblephus puniceus, a dominant fish on offshore reefs in the same region, interfered with spawning throughout the season and were observed to eat eggs when they were released. The spawning strategy ofC. nufar is similar to protogynous species in several respects, indicating that this functional gonochorist may not conform to current theoretical predictions.     

Brooding season, sex ratio, and brood pouch development in the seaweed pipefish, Syngnathus schlegeli, in Otsuchi Bay, Japan

Males of the seaweed pipefish, Syngnathus schlegeli, take care of their eggs in the brood pouch. These pipefish were periodically collected from the shallow seagrass beds in Otsuchi Bay on the Pacific coast of northern Honshu, Japan, from spring to autumn to investigate the basic reproductive ecology. Appearance of the pipefish in the coastal seagrass beds coincided with the initiation of reproduction. The reproductive season was from May to at least October, with its peak in July. A rearing experiment revealed that the brooding period of the male had a negative correlation with water temperature, and it was estimated to last about 1 month in the bay. Almost all males were brooding during the peak of the reproductive season. Although, the brood pouch of most males was either full or devoid of eggs, 6.2% of the males had a partially filled (20%–90%) brood pouch, and multiple clutches were identified in the brood pouch of some males, indicating that the mating system of the pipefish is polygamous, perhaps polygynous. Sex ratio fluctuated among months, and the overall sex ratio tended to be biased to male. Body size of males with an immature brood pouch had a wide range, from 133 to 215 mm standard length (SL). The smallest brooding male was 134 mm SL. Mean SL of brooding males was significantly larger than that of nonbrooding mature males. The number of males with an immature brood pouch was greater at the beginning than later in the reproductive season. The results seem to collectively indicate that the occurrence of a larger proportion of immature males at the onset of the reproductive season may be ascribed to both new recruitment and larger body size at maturation, resulting from the males trading the reproductive effort to somatic growth, perhaps to increase future reproductive success. Received: April 4, 2000 / Revised: September 21, 2000 / Accepted: January 16, 2001     

Optimal Mate Searching Strategy in the Symbiotic Spider Crab Inachus phalangium (Decapoda)

The reproductive strategy of the symbiotic spider crab, Inachus phalangium was studied from 1981 to 1983 in the natural environment. Main study focus was the efficiency of males in search of mates. I. phalangium females are site-constant, and live in the protection of one anemone or group. Males travel frequently between anemones harbouring females due to spawn; they copulate and guard the females until spawning, after which the male leaves again. A male operates in a patrol area containing 3–8 anemone groups and up to 8 females, visiting each female in turn repeatedly just before it is due to spawn. Patrol areas of different males may overlap, with resulting competition to fertilize a female's next brood. Large males have higher reproductive success than small ones. Females live up to 8 months after the moult of puberty and hatch up to six broods, and males live up to 7 months as adults. A male could fertilize a calculated 26,000 eggs, whilst a female's reproductive potential is ca. 4,200 eggs. Mortality risks are higher for males than for females, probably because of increased predation while leaving the protection of anemones in order to visit females. Males learn the positions of anemones harbouring females in their patrol areas, and when these are due to spawn. This allows a male to travel with a target and arrive punctually to fertilize the next brood due in his circuit. I. phalangium is the first marine invertebrate reported to use a “schedule” of localities and times for visiting prespawning females. In this way males minimize searching time and mortality risk, and maximize the number of broods fertilized.     

Song strophe-length and reproductive success in a non-passerine bird, the Hoopoe Upupa epops

Hoopoe Upupa epops males produce a very simple song, with a repertoire size of one, in which the main difference between different strophes of a male and between the songs of different males is the number of elements they include (strophe-length). In several passerine species it has been shown that strophe-length is a sexually selected trait that reflects male quality and correlates with reproductive success. Here we analyse whether in a non-passerine, the Hoopoe, strophe-length of males is correlated with several variables of their reproductive success. Females paired with males singing long strophes laid their first clutch earlier, produced larger first clutches and laid second clutches after a successful first one more frequently than those paired with males singing short strophes. Moreover, males with long strophes produced more fledglings in their first clutches and in the whole season, partly because they brought more food for the brood than males with short strophes. The relationships found are not mediated by age effects. Previously we have shown that Hoopoe females in the early spring are attracted preferentially to songs with long strophes. Here we show that males singing long strophes also obtain postpairing benefits in terms of reproductive success, and that females paired with these males obtain direct benefits because these males provide greater feeding effort in the second half of the nestling period. These findings support the hypothesis that in the Hoopoe, strophe-length is a sexually selected cue under direct selection.     

Steroid hormone profiles and correlative gonadal histological changes during natural sex reversal of sobaity kept in tanks and sea-cages

The gonadosomatic index of sobaity Sparidentex hasta fits well with the natural spawning season of February-March. At 12 and 24 months all the population matured as males. However, during this time, between April-September intersex gonads were seen. From October of the third year of life, females were seen for the first time. These changes in the histology of the gonads were correlated with the hormonal profile. Testosterone showed no significant correlation with sex but 11-ketotestosterone correlated very well with the mature male gonads and thus can be used for sexing. Oestradiol-17β higher in sex reversed individuals (females) in the spawning season than in males. The sequence of events in the protandrous sex change of this fish during the first two spawning seasons is male → intersex → male. However, during the third spawning season (age 36–37 months) this sequence is male →intersex → male or female (10–17%).     

Reproductive strategies in a partially protandrous shrimp,Athanas kominatoensis (decapoda: alpheidae): Sex change as the best of a bad situation for subordinates

An alpheid shrimp,Athanas kominatoensis, inhabiting a Japanese purple sea urchin was shown to be a partially protandrous hermaphrodite. They settled mainly in summer and spent the first reproductive season as males. Smaller males changed into females the following spring, but larger ones remained males throughout their lives. Sex change was socially controlled, as has been known in some fishes. In contrast to the fishes, however, subordinates changed their sex as the best of a bad situation in this shrimp. Most larger individuals lived singly or in sexual pairs, not tolerating others of the same sex on a host. The larger a male was, the more likely he was to be found with a female. On the contrary, males smaller than 3 mm were tolerated by larger males to some extent and had chances to cohabit and copulate with larger females. This made it advantageous to be functional as a male at first. Though the secondary sex change from female to male is theoretically expected, it is hardly realized because of the short life span. Hermaphroditism in this shrimp can be explained by the size-advantage model as a special case.     

Growth,reproduction, and feeding oF Fundulus heteroclitus (L.) on a North Carolina salt marsh

Fundulus heteroclitus (L.) from a North Carolina Spartina marsh teed largely on small crustaceans (amphipods, tanaids and copepods) and polychaetes. Fish longer than 30 mm standard length also ingested considerable amounts of living plant material. Smaller individuals were distinctly carnivorous. Recognizable particles of Spartina detritus occurred in less than 15% of the guts examined. The relationship of weight to length changed significantly during the year. Although females were larger than males of the same age. males were heavier than females of the same length, except for a brief period at the peak of the spawning season in the early spring. An average second season fish may lay up to 512 eggs from March through August, but first season fish did not reach reproductive size by the end of the spawning season. Growth of first season fish in mid-summer averaged 5% of their total weight per day. These significant seasonal changes in ecological properties of killifish populations are important in any estimates of growth, reproduction, and production.     

An experimental test on time constraint and sexual conflict over parental care

Because parental care is costly, a sexual conflict between parents over parental investment is expected to arise. Parental care behavior is an adaptive decision, involving trade‐offs between remating, and consequently desertion of the brood, and continuing parental effort. If the main advantage of desertion is remating, then this will be a time constraint, because the deserting individual will require a certain minimum period of time to breed again in the same breeding season. So, a short breeding season should force certain individuals to desert the first brood to have enough time to successfully complete their second breeding attempt. The rock sparrow, Petronia petronia, is an unusual species in which brood desertion can occur in both sexes and the breeding season is quite short so it is a good species to investigate the role of time constraint on brood desertion. For 3 years, I investigated the brood desertion modality of the rock sparrow. Then, for 2 years, I removed a group of experimental nest boxes during the autumn. Later, I re‐installed the experimental nest boxes after the start of the breeding season (2 weeks after the first egg was laid), mimicking a shortening of the breeding season for the (experimental) pairs that used experimental nest boxes. I found that in the experimental pairs, the percentage of deserting individuals was significantly higher than in the control groups, and the deserting individuals were older females. This experiment adds to our knowledge of timing of reproduction effects on individual decisions to desert by showing that a short and delayed breeding season may have different effects on males and females. To my knowledge, this is the first experimental study that demonstrates a direct link between time constraint and brood desertion.     

Why egg-caring males of Isaza (<Emphasis Type="Italic">Gymnogobius isaza</Emphasis>, Gobiidae) refuse additional females: preliminary field observations

Like many other gobies, males of the Isaza goby, Gymnogobius isaza endemic to Lake Biwa, Japan, conduct parental care of eggs at nests, and females are likely to choose mates while visiting nests. The reproductive strategy should induce polygyny, but Isaza males never accept additional females in one breeding cycle. Sampling data of broods indicated that the egg mass areas were much smaller than the nest sizes, suggesting that nest size is not the limiting factor in obtaining further eggs from additional females. The brood size greatly decreased as the duration of care progressed. Few individuals including caring males ate eggs, and heterospecific egg predators were rarely observed. Sixty percent of egg masses at the middle stages of egg development were infected with aquatic fungi, some being covered with a fungus mat that drastically reduced survivorship. Infected egg masses contained more eggs than non-infected ones at the same stage, indicating that large egg masses are prone to be frequently destroyed by fungi. It is likely that the activity of parental males is lowered during the long care periods at low water temperature in early spring. Such lowered activity of caring males might be responsible for infections in large broods that would have needed more care. We propose the hypothesis that male rejection of additional females may be related to optimal brood size, which will be less susceptible to fungus infection and produce more hatching young than otherwise. This hypothesis will explain not only male avoidance of additional females but also some unique reproductive behaviors of this fish such as some females spawning of a portion of of the mature eggs in one nest.     

Sound production and associated behavior in a cichlid fish,Cichlasoma centrarchus. II. Breeding pairs

Synopsis Pairs of Cichlasoma centrarchus were observed daily in the laboratory. Both males and females made sounds during a breeding cycle but all sounds were aggressive in context; no sounds were heard to accompany courtship. Males made more sounds before spawning than afterwards and these were associated with territorial defense and with establishment of dominance over the female. Females produced more sounds after spawning than before, most in the context of brood defense but some toward the male during pre-spawning nest preparation. Prior to spawning, the number of sounds made by the males toward their mates increased but the aggressive actions accompanying them became less intense. No such inverse correlation of agonistic intensity with number of sounds made was found for the females. From this study and earlier ones by the author it was concluded that sound in this species is a threat display which 1) provides an expression for agonism alternative to the performance of actions which could injure the female or drive her away, and 2) lessens the risk of injury to male or female during territory or brood defense.     

Seasonal changes in reproductive and physical condition, sexual dimorphism, and male mating tactics in the jewelled blenny Salarias fasciatus

To investigate seasonal changes in reproductive and physical condition, sexual dimorphism, and mating tactics in the jewelled blenny Salarias fasciatus, monthly collections were conducted on the fringing reef in northern Okinawa, Japan. Monthly variation in the female gonadosomatic index suggested that the breeding season of this species is from April to June. The physical condition and hepatosomatic index of both sexes considerably deteriorated during the course of the breeding season. Such declines may be primarily due to egg production in females and brood care in males. Males’ elongated anal spines were longer than females’, but no other apparent sexual dimorphisms were detected, indicating that S. fasciatus exhibits a low degree of sexual dimorphism. Examinations of testes size and the testicular gland area during the estimated breeding season revealed that the gonadosomatic index values of smaller males did not differ from those of larger males. This result may differ from other blenny species that exhibit alternative male reproductive tactics. However, patterns of male testicular glands of S. fasciatus were similar to those of other blennies with alternative tactics, i.e., smaller males had poorly developed testicular glands compared with larger males.