Group spawning results from the streaking of small males into a sneaking pair: male alternative reproductive tactics in the threespot wrasse Halichoeres trimaculatus

In many protogynous wrasses, large males with bright coloration (terminal phase males, TP males) establish mating territories and pair-spawn with females. In contrast, small primary males with drab coloration (initial phase males, IP males) are non-territorial and adopt three alternative reproductive tactics—group spawning, streaking, and sneaking. We investigated how IP males of the threespot wrasse Halichoeres trimaculatus use these tactics in different situations. The mating frequency of the IP males was positively correlated with their courtship frequency, but not with their body size. Larger IP males tended to attack the smaller ones at the mating sites. This indicates that the larger IP males attempted to exclude the smaller ones from mating with the intention of minimizing the number of IP males involved in group spawning and ultimately leading to pair spawning (sneaking). However, the larger IP males were unable to completely exclude the smaller males because the intensity of the attack by the larger IP males was weak. Consequently, the smaller IP males could easily streak into the sneaking of larger IP males, thereby resulting in group spawning.     

Interspecific variation in spawning time and male mating tactics of the parrotfishes on a fringing coral reef at Iriomote Island,Okinawa

Spawning time and male mating tactics of parrotfishes (family Scaridae) were investigated on a fringing coral reef at Iriomote Island, Okinawa. Spawning was observed in 14 species, and more frequently in more abundant species such as Chlorurus sordidus, Scarus rivulatus and Chlorurus bowersi. At the reef-edge spawning site, C. bowersi spawned at high tide, C. sordidus spawned both at high tide and in the early morning, whereas Calotomus carolinus and most of the Scarus species such as S. rivulatus spawned only in the early morning, mostly 0630–0830 h. Spawning only in the early morning irrespective of tide phase and moon age has seldom been reported from the scarid species of other localities. It is suggested that spawning in the early morning would be adaptive in species such as S. rivulatus, which migrated considerable distances (ca. 500 m) to the inshore feeding sites, in order to minimize feeding losses due to migration. For male mating tactics, pair spawning by territorial TP (terminal phase) males occurred in all 14 species, and streaking and group spawning by nonterritorial small IP (initial phase) males were seen more frequently in more abundant species. Moreover, group spawning by nonterritorial TP males, which were larger than the IP males but smaller than the territorial TP males, frequently occurred in S. rivulatus. Such mating tactics of TP males have not been reported from Scaridae.     

Alternative male mating tactics of the endemic Red Sea parrotfish Scarus ferrugineus

The present study shows that small non‐territorial terminal‐phase males of the rusty parrotfish Scarus ferrugineus are reproductively active and are comparable with initial‐phase males in behaviour, rates of participation during group‐spawning and success in streaking into pair spawning. Large territorial terminal‐phase males defend contiguous territories for several hours during the morning where they pair spawn with initial‐phase females.     

Social control of terminal phase transition in primary males of the diandric wrasse, <Emphasis Type="Italic">Halichoeres poecilopterus</Emphasis> (Pisces: Labridae)

In many diandric fishes, large territorial males with bright body coloration (terminal phase (TP) males) are derived either from initial phase (IP) females that change sex to male or from IP primary males that change color and behavior, but do not change sex. The mechanism controlling the transition of IP primary males into TP males is not well understood. We conducted cohabitation experiments to examine social conditions favoring TP transition by primary males in the diandric wrasse, Halichoeres poecilopterus. IP primary males always started TP-specific sexual behavior in the presence of a smaller subordinate, and subsequently acquired TP body coloration. In contrast, primary males under subordinate conditions often performed female-like sexual behavior. In pairs with similar body sizes, both individuals initiated TP male behavior. The results suggest that TP transition in primary males may be closely related to a dominance relationship (or size order) within social groups, as it is in the case of sex change by females.     

Local variability in population structure and density of the protogynous reef herbivoreSparisoma viride

Synopsis We compare the (relative) abundance of life phases [juveniles (JU), initial phase (IP) and terminal phase (TP) fish], social categories (territorial and group adults), and fish following alternative mating styles, in three local populations of the protogynous reef herbivore,Sparisoma viride, on the fringing reef of Bonaire (Netherlands Antilles). In order to determine the adaptive significance of variations in social organization, they are related to the density of conspecifics and other herbivores and to the availability of food, shelter and mating sites. The most striking difference is the high abundance of JU and group fish at one location (Playa Frans) and the total absence of group fish at another (Red Slave). These differences are coherent with a gradient in population density, total herbivore density, scarid grazing pressure, and reproductive output, all of which are highest at Playa Frans and lowest at Red Slave. Exposure to waves and currents shows an inverse trend. The differences in the relative abundance of territorial fish can be explained by the concept of economic defendability, which is reduced at higher population density. In a life history context, small TP group males represent bachelors that sacrifice current reproduction for better future prospects. As predicted by life history theory, early sex change is promoted at sites where the future rewards are higher (higher spawning rates of large TP males) and where the costs incurred during the bachelor phase are reduced (more spawning opportunities for group TP males). At Red Slave an alternative male mating style (streaking) appears to be promoted by the lack of a refuge for group TP males and by a dense gorgonian canopy, allowing IP males to reside inside territories. We conclude that most observed differences in population structure can be considered adaptive in an ecological and in a life history context. Population density is a major factor in both contexts. Analysis of the variability in adult density in relation to JU density and the availability of food and shelter indicates that theS. viride populations at Bonaire are not totally controlled by stochastic processes. Considering the small spatial scale and the high dispersal of the planktonic embryos and larvae, the observed variability in behavioural and life history traits ofS. viride points to a high degree of phenotypic plasticity.     

Mating patterns of female Leon Springs pupfish Cyprinodon bovinus

In a field study of Leon Springs pupfish Cyprinodon bovinus, two questions about female promiscuity were investigated. First, were females selective in the males with whom they spawned or were they unselective, spawning randomly among males? Second, how promiscuous were the females, i.e. with how many males did they spawn? If simply spawning with many males maximized a female's reproductive success, then females might be expected to spawn randomly with as many males as possible. Alternatively, if females were selective but engaged in multiple mating, they would limit their spawning to preferred males. In the only wild population of this endangered fish, breeding males defend closely associated territories in the shallow margins of a single desert pool. No territories were observed elsewhere in the pool. Therefore, all territorial males were present simultaneously and females could survey all of them, depositing any number of eggs with one, a few or many males. Rather than spawning randomly, females surveyed many males first, visited relatively few males and ultimately spawned with a small fraction of those available males. With increasing numbers of spawns, however, females increased the number of different mates with whom they spawned. Thus, females showed a bet‐hedging tactic of having a narrow mate preference while also laying eggs in the territories of other males, possibly to reduce egg predation and to avoid inbreeding.     

Male Parasitic Spawning in Two Species of Triplefin Blenny (Tripterigiidae): Contrasts in Demography, Behaviour and Gonadal Characteristics

Axoclinus nigricaudus and A. carminalis are blennioid fishes from the Gulf of California, Mexico. Males show alternative mating tactics; territorial individuals attract females while non-territorial individuals parasitically spawn with territorial males' females. Demography and gonadal characteristics were related to the degree of parasitic spawning (sperm competition) within and between species. Males of both species showed bimodal size distributions that largely reflected the two tactics. Territorial males spawned much more frequently than non-territorial males, but parasitic spawning was significant. Non-territorial males were more common and rates of parasitic spawning were much higher in A. nigricaudus indicating that it experienced higher sperm competition. In agreement with sperm competition theory, relative testis weight was greater in A. nigricaudus. In A. nigricaudus, the majority of parasitic matings were by non-territorial males, whereas in A. carminalis, both male-types parasitised frequently. Accordingly, only in A. nigricaudus did non-territorial males have relatively heavier testis than territorial males. In both species the testicular gland, that produces accessory products for sperm transfer, was large in territorial males, but small or undeveloped in non-territorial males suggesting male-types differ in fertilisation mode.     

The relative costs and benefits of territorial defense and the two conditional male mating tactics in the Comanche Springs pupfish (Cyprinodon elegans)

We examined the aggressive costs and reproductive benefits of territorial defense and its alternatives in a population of the Comanche Springs pupfish (Cyprinodon elegans). The breeding system was characterized by three different male mating tactics: territorial defense, satellite positioning, and sneak spawning. The mating tactic adopted by males reflected the males' sizes. Territorial residents were the largest, satellites were medium-sized, and sneakers were the smallest adult males observed. Consistent with the hypothesis that primary mating tactics are relatively high-cost, high-benefit strategies, we found that territorial males engaged in a number of aggressive encounters but had higher reproductive successes than any other males. However, our observations did not support the premise that conditionally breeding males engage in relatively low-benefit, low-cost tactics. Medium satellites and small sneakers acquired fewer spawns than did territorial males, but both satellites and sneakers were involved in as much aggression as territorials. That is, the data supported the prediction that satellite or sneaker males with the inability to compete for territories would attempt to accrue some reproductive opportunities in the presence of territorial males despite the high costs of spending time on the breeding grounds. Adopting conditional tactics appeared to allow satellites and sneakers to make the best of a bad situation. During a subsequent breeding season, large males were absent from the population, and medium-sized males established territories. The aggressive behavior exhibited by medium residents was similar to the previous year, but these males did not acquire higher reproductive successes than medium satellites had. The implications of switching tactics and the influence of operational sex ratios on the costs and benefits of the male tactics are briefly addressed. Electronic Publication     

Pre-oviposition Ejaculation in Externally Fertilizing Fish: How Sneaker Male Rose Bitterlings Contrive to Mate

Pre-oviposition ejaculation as a mating tactic of sneaker males in the rose bitterling, Rhodeus ocellatus, was studied under natural and artificial conditions. In a small pond in Yao city, Osaka, Japan, the operational sex ratio of males and females was found to be approximately 3.5:1 and the proportion of males to the mussels, which serve as spawning beds for the rose bitterling, was approximately 2:1. Competitively subordinate rose bitterling males which spawned into the mussels participated in mating by sneaking, because not all males could occupy territories around the mussels. The sneaker males often released sperm not only after but also before egg-laying (this ejaculation movement by the male before egg-laying is termed ‘pre-oviposition ejaculation’). In pair spawning with sneaker, the sneakers frequently performed pre-oviposition ejaculations, which territorial males never performed. In the field, pre-oviposition ejaculations by sneakers coincided with the leading of females by territorial males. Under artificial conditions, I demonstrated by using electrophoretic paternal analyses that the pre-oviposition ejaculations by the sneakers were more effective than the post-oviposition ejaculations by the territorial males. In addition, there were negative size-dependences in ejaculation achievement rate and fertilization success of the sneaker males.     

Reproductive Success Associated with Territoriality, Sneaking, and Grouping in Male Rose Bitterlings, Rhodeus ocellatus (Pisces: Cyprinidae)

The spawning success of male rose bitterlings, Rhodeus ocellatus, adopting an alternative reproductive style, was estimated through behavioural data and electrophoretic paternal analyses in field observations and experiments. Three mating patterns were observed: territoriality, sneaking, and grouping. Mating patterns depended on a male's relative size and on local male density (the number of males around a spawning spot: a mussel). Spawning patterns (pair spawning, pair spawning with sneaker, and group spawning) varied with local male density. Time-budget data of the territorial males indicated a trade-off between chasing and courtship behaviour as local male density changed. Females deposited appoximately only 1 egg per egg-laying into the mussels. As a result of isozyme analysis, a minimum of 12% (two out of 17) of the offspring in the sample were found to have been fathered by sneaker males in pair spawning with sneaker. I scored through behavioural data the mating success per spawning for each pattern, on an individual basis. The average reproductive success per spawning for each pattern was: territorial (0.61), sneaking (0.31) and grouping (0.11), and thus the successes of the patterns were not equal. Accordingly, the alternative reproductive styles of male rose bitterlings are best interpreted as alternative phenotypes in a conditional behaviour.     

The effect of alternative mating tactics on the fertilization success of a hermaphroditic seabass

In the simultaneously hermaphroditic marine fish, Serranus subligarius, male role individuals are known to pair spawn, group spawn and streak spawn. While the effects of these common mating tactics on mating success in the male role have been well studied, their consequences for the reproductive success of the individuals taking the female role have received little attention. To investigate those consequences, I observed mating behaviors and quantified fertilization success in natural and experimental settings during the summers of 2005-2008 at three sites with different local population densities. I observed focal individuals in 15-min increments and recorded the total number of spawns, number of streak spawns, size of participating spawners, and fertilization rate. The occurrence of small-sized individuals in the local population is associated with higher frequencies of streaking behavior; these small fish are most often first-year individuals reaching sexual maturity late in the spawning season (August/September). Spawns that included one or more streak spawners had a significantly lower average fertilization rate (89?%) than pair spawns without a streak spawner (97?%). This pattern was confirmed with a field manipulation experiment in which spawning events that included streakers again showed lower fertilization rates (93?%) than spawning events that did not include streakers (98?%). These lower fertilization rates occurred despite the fact that spawns that included multiple males produced, on average, 20?% more sperm than produced in spawns with only a single male. These results indicate that females incur a significant fitness cost when streakers invade a spawning event, a cost not attributable to sperm limitation or any direct effects on the female.     

Bigamy or monogamy with maternal egg care in the triggerfish,Sufflamen chrysopterus

Reproductive behavior and mating systems of the triggerfish,Sufflamen chrysopterus (Balistidae), were studied on the fringing reef of Sesoko Island, Okinawa. Both males and females maintained territories against consexual adults, feeding on benthic animals within their own territories. Each male territory overlapped one or two female territories, with mating occurring between the cohabitants. The monogamous males were smaller and foraged more frequently than the bigamous ones, suggesting that the former allocated more energy to growth rather than to improving reproductive success. Pair spawning occurred around sunrise, females only taking care of the demersal eggs until hatching, which occurred around sunset of the same day. On spawning days females foraged less frequently than usual, but as frequently as males. Females spawned at intervals of 5–7 days, usually shifting sites within their territories. Thus both feeding and spawning sites were available for females within their territories, providing males with the opportunity to monopolize females by defending their territories.     

Social Behavior of Males and Simultaneous Hermaphrodites in the Lantern Bass

Serranus baldwini (Serranidae), the lantern bass, is a small, gleaning carnivore found in turtle grass and rubble substrates in the Caribbean. Small S. baldwini are simultaneous hermaphrodites, but large members of this species are males. The males patrol territories in which several hermaphrodites reside. Hermaphrodites spawn as females with the resident males and rarely spawn as males themselves. Unlike the pattern in reciprocating hermaphrodites, courtship is largely a male function in S. baldwini. Males are much more active and aggressive than are hermaphrodites. In reciprocally spawning species, interactions among mates are more symmetrical. The behavior patterns found in the serranines reflect the differences in mating systems in a manner similar to that found in other organisms and is consistent with current mating system theory.     

Spawning behavior and haremic mating system in the corallivorous butterflyfish,Chaetodon trifascialis, at Kuroshima Island, Okinawa

Territorial and spawning behavior ofChaetodon trifascialis were investigated on a small patch of reef at Kuroshima Island, Okinawa, Japan. Three males and 8 females inhabited the reef, each individual defending a territory against conspecifics of the same sex. Each male territory included 2 or 3 female territories. In the daytime, each male frequently visited the females living in its territory. At dusk in the full or new moon periods, courtship began within the female territories, pair spawning subsequently occurring within or near those territories. When a male actively courted a female in the territory of a second male, the latter male immediately chased off the intruder. Thus, mating occurred only between a male and females living in former's territory. This is the first report of a haremic mating system among butterflyfishes (Chaetodontidae).     

Territory re‐establishment in Cyprinodon variegatus lacepede

Cyprinodon variegatus males were allowed to establish territories in small aquaria. The ability of a male to maintain a territory was examined under conditions that varied group composition and sequentially varied space availability. Three cohorts of males were identified: non‐territorial individuals, rarely territorial individuals, and frequently territorial individuals. The results indicate that group social structure is not affected by changes in available space. Although no single male was always territorial in trials that varied group composition, a small number of males were frequently territorial. Often these successful males were temporarily displaced, but they typically regained a territory in subsequent trials.     

Male dimorphism, territoriality and mating success in the tropical damselfly, Paraphlebia zoe Selys (Odonata: Megapodagrionidae)

The tropical damselfly Paraphlebia zoe has two male morphs: a black-winged (BW) male which is associated with territorial defense of oviposition sites; and a hyaline-winged (HW) male similar in appearance to females, and, compared to the black morph, less frequently found defending territories. In a wild population of this species, we first assessed the relationship between phenotypic traits [male morph, size and territorial status (being territorial or non-territorial)], their role on mating success, and the degree to which a particular territory may contribute to male mating success. Second, to relate a physiological basis of being territorial we compared both morphs in terms of muscular fat reserves and thoracic muscle, two key traits related to territory defense ability. Males of both morphs defended territories although the BW males were more commonly found doing this. BW males were larger than HW males and size predicted being territorial but only within HW males (territorial males were larger) but not in BW males. Male mating success was related to territorial status (territorial males achieved a higher mating success), but not to morph or size. Furthermore, territory identity also explained mating success with some territories producing more matings than others. The BW morph stored more fat reserves which may explain why this morph was more likely to secure and defend a place than the HW morph. However, the HW morph showed higher relative muscle mass which we have interpreted as a flexible strategy to enable males to defend a territory. These results are distant to what has been found in another male dimorphic damselfly, Mnais pruinosa, where the advantage of the non-territorial morph relies on its longevity to compensate in mating benefits compared to the territorial morph.     

Diurnal periodicity of spawning activity of permanently territorial damselfishes (Teleostei: Pomacentridae)

Synopsis Like other congeneric damselfishes, the herbivorous Stegastes altus defends individual feeding territories from heterospecific food competitors, regardless of sex. Females spawned demersal eggs for 31.4 min (n = 25) at the nest in territories of males 0–75 m away from theirs. Throughout the spawning season (June to September), spawning occurred only at dawn, mainly just after sunrise. Daily activity of the fish community showed that potential diurnal food competitors were few or inactive only at dawn and dusk. The frequency of intrusions into the female's territory by heterospecific competitors were as low when she left her territory to spawn at dawn, as they were in the daytime when she defended it. Removal of the female in the daytime resulted in a significant increase in intrusion frequency. An ‘anti-competitor hypothesis’, whereby dawn spawning ensures the food resource in the female's territory seems to explain not only the spawning periodicity in S. altus but also the timing of spawning of other permanently territorial damselfishes. Contribution from the Laboratory of Animal Ecology, Kyoto University, No. 492.     

Do Feeding Resources Induce the Adoption of Resource Defence Polygyny in a Lekking Butterfly?

Among polygynous species, males often compete for the possession of mating sites to increase their reproductive success. Weaker individuals frequently adopt alternative non‐territorial mate‐locating tactics, but the adoption of alternative territorial tactics may also occur. Although alternative tactics with territory defence are less common in arthropods, factors that drive its adoption may provide information to understand the organization of different territorial mating systems in the group. Here we investigate the adoption of resource‐based territoriality as an alternative to a non‐resource‐based one by males of the butterfly Paryphthimoides phronius. Male P. phronius commonly defend sunny clearings lacking feeding resources in the forest edge (non‐resource‐based territoriality). However, after experimentally offering fermenting fruit in previously undefended sites, we showed that males also adopt a resource defence tactic. Males in territories with fermenting fruits apparently feed on this resource when they are not defending the territory. However, males in sites without resources did not migrate to territories with resources when given the opportunity. To our knowledge, this is the first experimental investigation to show a non‐resource‐ and an alternative resource‐based mate‐locating tactic in a butterfly. We suggest that this behavioural flexibility may represent an important step to understand the ecological factors responsible for the organization and evolution of different territorial mating systems in insects.     

Courtship displays and coloration as indicators of safety rather than of male quality : the safety assurance hyposthesis

Male courtship displays and bright coloration are usually assumedto provide information to females about some aspect of themale's value as a mate. However, in some species, courtshipmay serve another function—namely, indicating the currentpredation risk at the mating site and assuring the female thatit is safe to mate there at this time. We developed this safetyassurance hypothesis (SAH) and tested its predictions in thebluehead wrasse (Thalassoma bifasciatum), a Caribbean reef fish. Females in this species come to males' territories to spawn,and males court each arriving female. Males with larger whiteflank patches court less intensely than less bright males.We show that such males are probably more visible to predatorsand thus need not court so intensely to provide the same degreeof safety assurance to a female. When model lizardfish predatorsare presented at spawning sites, males habituate to them quickly,but newly arriving females who see the predator are expectedto demand more assurance of site safety. Accordingly, and consistentwith the SAH, males court females more intensely (longer averagecourtship bout length) under such circumstances, but maleswith bright flank patches do not increase their courtship asmuch as duller males do. Despite this relatively low intensityof courtship, the spawning rate of bright males does not declinerelative to that of duller males in the presence of a predator,suggesting that bright coloration conveys a differential benefit.Females of species like the bluehead wrasse, who spawn repeatedlyover the course of their life, are expected to be more concernedwith their own risk of mortality during each spawning boutthan with the quality of a particular male. It is in such speciesthat we expect the SAH to be most applicable.