The costs of reproduction to males and females of a paternal mouthbrooding cardinalfish Apogon notatus

In the cardinalfish Apogon notatus , starving males mouthbrood the eggs, and females are more active than males in courtship and in attacks against conspecific intruders upon their breeding territory, but sexual ornaments are developed in males. Condition factor, hepatosomatic index and fat body-somatic index declined in both sexes during the breeding season. The deterioration of somatic condition was more severe in females, suggesting that the overall energetic costs were larger for females which produced more than twice as many clutches as males brooded in a season. Selective mortality of females could be due primarily to the depletion of their energy reserves. The increased mortality in females is a possible mechanism for the male-biased operational sex ratio which may provide the potential for sexual selection on males.     

Nocturnal hatching timing of mouthbrooding male cardinalfish Apogon niger

We observed hatching behavior by mouthbrooding males of the cardinalfish, Apogon niger. Mouthbrooding males showed no feeding activities at night, in spite of their nocturnal feeding habit. On the day of hatching, they released newly hatched larvae from their mouths on average 81 min after sunset. Semilunar hatching periodicity was significant, but its diel pattern was independent of the tidal rhythm. Sunset hatching may be advantageous not only to offspring because of their low predation risk but also to parental males because they can resume feeding sooner, thereby reducing the energetic loss from fasting while mouthbrooding. Received: August 22, 2000 / Revised: November 28, 2000 / Accepted: January 12, 2001     

Seasonal pattern of filial cannibalism by Apogon doederleini mouthbrooding males

In temperate waters of southern Japan, mouthbrooding males of the cardinal fish Apogon doederleini sometimes ate their entire brood within a day of spawning. In spite of annual variation in age structure and length of the breeding season, however, the annual cannibalism rate (broods cannibalized to total broods spawned) was nearly constant, 12–16%. Fish 1 year old frequently cannibalized early broods of the season, especially the first brood, whereas the cannibalism rate by 2 year-old fish did not vary within the season. In contrast, the cannibalism by older males increased late in the season. This tendency was attributed to their different allocation patterns to growth and reproduction. For 1 year-old fish, which can enhance future reproductive success by growth and cannibalizing on early broods instead of mouthbrooding (at relatively low temperatures), this may be a tactic for investing energy in growth. For fish 3 years, which have more breeding cycles and grow little, cannibalizing late broods may be energetic compensation for their poor somatic condition. No seasonal variation of cannibalism by 2 year-old fish can be explained by their intermediate nature of growth and reproduction. Multiple mate availability is one factor facilitating the cannibalism by 2 and 3 + year-old fish whose operational sex ratio is female-biased.     

Characterization and isolation of DNA microsatellite primers in the cardinalfish (Apogon doederleini)

Proper management of reef areas depends greatly on understanding the degree of dispersal of each species involved. The larvae of most reef fishes disperse from the natal reef before or soon after hatching and return to the reef environment after a pre‐settlement stage of several days to weeks. We characterized eight polymorphic microsatellite loci for the cardinal fish Apogon doederleini to study the spatial scale of connectivity of populations of different reefs of the Great Barrier Reef, Australia.     

Male ornamentation and its condition-dependence in a paternal mouthbrooding cardinalfish with extraordinary sex roles

Cardinalfishes, in which males alone provide mouthbrooding, are likely candidates for sex-role reversal because of a higher potential reproductive rate for females than for males. In the gregarious cardinalfish, Apogon notatus, females establish breeding territories to form pairs prior to the breeding season. Within breeding pairs, females are more active in courtship and in attacks against conspecific intruders. Sex roles thus seem to be behaviorally reversed. The operational sex ratio is, however, male-biased because females suffer higher mortality than males and consequently males predominate in number in the adult population, leading to the prediction that males would be sexually selected. In the present study, morphological measurements showed that males had a protrudent lower lip that was expressed markedly during the breeding season. Field observation revealed that males with a longer and wider lip were preferentially accepted as a mating partner by territorial females. The male lip size positively correlated with their somatic condition, suggesting that the ornamental lip has evolved through indicator mechanisms of sexual selection. By contrast, females had longer fins than males, but these sexual dimorphisms were less pronounced and most of them were seasonally constant. These results support the prediction that sexual selection acts on males in this fish. Electronic Publication     

Filial cannibalism by mouthbrooding males of the cardinal fish,Apogon doederleini, in relation to their physical condition

Synopsis Paternal brood cannibalism was observed in a population ofApogon doederleini in Shikoku Island, Japan. Of 361 egg masses mouthbrooded by males, 47 disappeared within a day of spawning. A stomach check with a syringe ascertained that they had been consumed by the males. The frequency of this cannibalism increased as the breeding season advanced. As males completed 4–7 breeding cycles in a breeding season and spent 80% of the time mouthbrooding without taking ordinary food, their physical condition deteriorated greatly late in the breeding season. We concluded that parental physical condition is an important factor in the occurrence of brood cannibalism.     

Social and reproductive behavior of three mouthbrooding cardinalfishes,Apogon doederleini,A. niger and A. notatus

Synopsis Social and reproductive behavior of three paternal mouthbrooding cardinalfishes (Apogonidae) were investigated in the shallow marine waters of Shirahama, Japan. The solitary species Apogon doederleini and A. niger bred in transient pairs, in which a male and female associated for only a few hours of each afternoon on less than 5 successive days. The prespawning behavior was the same as the courtship display on days prior to spawning. After spawning, egg-incubating males were usually left alone. The gregarious species Apogon notatus formed territorial lasting pairs, which resided at given sites from dawn to dusk on each day during a period of a month or more. After spawning, the egg-incubating male either continued to stay with his mate in the territory, or left it to enter into an aggregation. In the latter case, the female continued to reside in the territory, pairing with a new male whom she brought from an aggregation. It is suggested that in paternal apogonids the prolonged pair bond and territoriality should have developed only in gregarious species as secondary adaptation for reproductive success: to avoid conspecific interference during spawning.     

Apogon selas,a new cardinalfish from the western Pacific

A new species of cardinalfish,Apogon selas, is described from 27 specimens from New Guinea, Ryukyu Islands, and Philippines; also known from photographs taken in the Solomon Islands and Indonesia. It is a species of the subgenusOstorhinchus Lacepède, distinctive in having a first dorsal fin of VII spines, 13 pectoral rays, 14–19 gill rakers, smooth preopercular ridge, body depth 2.9–3.6 in SL, and a color pattern of a black spot as large as the eye centered on the caudalfin base and two dusky stripes (mainly red or golden in life), one midlateral and the other from tip of lower jaw across cheek to thorax.A. selas appears to be most closely related toA. endekataenia Bleeker which differs in having 14 pectoral rays, 18–21 gillrakers, and six dark stripes on the body.     

Determinate growth in a paternal mouthbrooding fish whose reproductive success is limited by buccal capacity

The life history of the paternal mouthbrooding cardinal fish Apogon doederleini was investigated in the temperate waters of Japan, with particular reference to its growth and reproductive rate. Both males and females almost ceased to grow at age 3 years, although living to 7 years of age. Their growth pattern, represented by the relative size at sexual maturity to the asymptotic size and the von Bertalanffy growth coefficient, was among the most determinate in ectothermic vertebrates. Brood size just before hatching increased in proportion to the second power of the body size of the brooding male, and correlated more positively with the male's than the female's body size, suggesting that it was limited by the male's buccal capacity. The estimated total number of broods hatched in a breeding season showed a weak or no correlation with the body size or age in either sex. Using life-history parameters based on data of A. doederleini, a simulation model of energy allocation without considering sexual interaction revealed that the optimal growth pattern shows an indeterminate growth that differs greatly from the actual growth pattern of A. doederleini. This suggests that there are some brooding constraints to size-advantage of reproductive success in this species. The possible mechanism of such reproductive constraint is discussed.     

Molecular phylogeny and stripe pattern evolution in the cardinalfish genus Apogon

Cardinalfishes of the genus Apogon (Apogonidae) are one of the most speciose (>200 species) and numerically dominant fishes in coral reefs. Although the genus is divided into 10 subgenera, more than 70% of the species are included in the subgenus Ostorhinchus, most having either horizontal or vertical lines on the body. The phylogenetic relationship among 32 species of subgenus Ostorhinchus and 11 species of four other subgenera of Apogon, based on mitochondrially encoded 12S and 16S ribosomal genes and intervening tRNA(Val) gene, were investigated, using two species of the apogonid genus Fowleria as outgroups. The analyses demonstrated that Ostorhinchus (the most speciose subgenus) was polyphyletic, comprising at least three lineages, Ostorhinchus I, II, and III. Ostorhinchus I included two species, A. (O.) amboinensis and A. (O.) sangiensis, being a sister group to subgenus Zoramia. Ostorhinchus II and III included species with horizontal and vertical lines on the body, respectively. The respective monophylies of the latter two groups, together with a molecular clock calibration, indicated that in the evolutionary history of the genus, basic stripe patterns evolved first (more than 20 million years BP), with subsequent pattern diversification and modification.     

Diverse parentage relationships in paternal mouthbrooding fishes

While mouthbrooding is not an uncommon parental care strategy in fishes, paternal mouthbrooding only occurs in eight fish families and is little studied. The high cost of paternal mouthbrooding to the male implies a low risk of investment in another male''s offspring but genetic parentage patterns are poorly known for paternal mouthbrooders. Here, we used single-nucleotide polymorphism genetic data to investigate parentage relationships of broods of two mouthbrooders of northern Australian rivers, mouth almighty Glossamia aprion and blue catfish Neoarius graeffei. For N. graeffei, we found that the parentage pattern was largely monogamous with the brooder male as the sire. For G. aprion, the parentage pattern was more heterogeneous including observations of monogamous broods with the brooder male as the sire (73%), polygyny (13%), cuckoldry (6%) and a brood genetically unrelated to the brooder male (6%). Findings demonstrate the potential for complex interrelationships of male care, paternity confidence and mating behaviour in mouthbrooding fishes.     

Breathing with a mouth full of eggs: respiratory consequences of mouthbrooding in cardinalfish

Mouthbrooding occurs among several groups of fishes. Although a mouth full of eggs can be expected to pose a considerable respiratory problem, to our knowledge no study has examined respiratory consequences of mouthbrooding in fishes, or how hypoxia or strenuous swimming may affect the success of this reproductive strategy. In two species of cardinalfish (Apogon fragilis and Apogon leptacanthus), from the reef at Lizard Island (Great Barrier Reef), we found that mouthbrooding significantly reduced the ability to take up oxygen at low ambient oxygen levels. While the direct energetic cost of mouthbrooding appeared insignificant at rest in well-oxygenated water, mouthbrooding significantly reduced the respiratory scope of the fishes and their capacity for sustained aerobic swimming. The males spat out their eggs in hypoxia. Interestingly, the species with the larger brood, A. fragilis, spat out the brood at a higher water [O2] than did A. leptacanthus, which had a smaller mean brood mass. Moreover, in contrast to mouthbrooding A. leptacanthus, mouthbrooding A. fragilis was unable to increase its ventilatory frequency in response to hypoxia. This suggests a trade-off situation between hypoxia tolerance and brood size. Apparently, A. fragilis has sacrificed hypoxia tolerance in favour of a large brood size to a greater extent than has A. leptacanthus.     

Male size determines reproductive output in a paternal mouthbrooding fish

Size can have strong effects on reproductive success in both males and females, and in many species large individuals are preferred as mates. To estimate the potential benefits from mate choice for size in both sexes, I studied the effects of the size of each sex on the reproductive output of pairs of Banggai cardinalfish, Pterapogon kauderni, a sexually monomorphic obligate paternal mouthbrooder. When pairs were allowed to form freely, a size-assortative mating pattern was observed and larger pairs had a higher reproductive output as determined by total clutch weight and egg size. To separate the potential benefits from mate choice for size for each sex, I subsequently used these pairs to form reversed size-assortative pairs, that is, the largest male paired to the smallest female and vice versa. I found a positive correlation between male size and clutch size: relatively heavier clutches were found in pairs where females were given a larger male. This suggests that the size of the male influences clutch weight. For egg size, however, the size of both sexes seemed important. The study reveals the benefits of mutual mate choice on size in this species: larger females provide larger eggs and larger males can brood heavier clutches. Furthermore, these results suggest that females differentially allocate resources into the eggs according to the size of the mate.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Filial cannibalism as a conditional strategy in males of a paternal mouthbrooding fish

Filial cannibalism is widespread in a variety of animal species and has been generally accepted as an adaptive behavior. Within a population, some individuals adopt filial cannibalism and others do not, in spite of its adaptiveness. There is little knowledge of how such a polymorphic trait is maintained in nature. To understand the underlying mechanism of cannibalistic polymorphism, we conducted a long-term field study that involved monitoring of the reproductive experience of marked individuals in the paternal mouthbrooding cardinalfish, Apogon doederleini, in which parental males sometimes cannibalize their entire broods. We assumed that filial cannibalism can be described as one of three possible strategies: alternative, mixed or conditional. Individual cannibalistic tendencies, represented by the number of entire brood cannibalism performed by each individual in one breeding season, showed a random distribution within the study population. Moreover, the individual cannibalistic tendencies were not consistent between two successive seasons. These results suggest that filial cannibalism is phenotypically plastic, thus eliminating the alternative strategy as a possible mechanism. Comparison of variance in reproductive success between cannibals and non-cannibals showed that observations were not in accordance with those expected in the case that males adopt filial cannibalism stochastically, that is, as a mixed strategy. Our previous studies have indicated that filial cannibalism is affected by male status, such as age, somatic condition and mate availability. In conclusion, filial cannibalism by male A. doederleini is carried out as a conditional strategy.     

Females produce larger eggs for large males in a paternal mouthbrooding fish.

When individuals receive different returns from their reproductive investment dependent on mate quality, they are expected to invest more when breeding with higher quality mates. A number of studies over the past decade have shown that females may alter their reproductive effort depending on the quality/attractiveness of their mate. However, to date, despite extensive work on parental investment, such a differential allocation has not been demonstrated in fish. Indeed, so far only two studies from any taxon have suggested that females alter the quality of individual offspring according to the quality/attractiveness of their mate. The banggai cardinal fish is an obligate paternal mouth brooder where females lay few large eggs. It has previously been shown that male size determines clutch weight irrespective of female size in this species. In this study, I investigated whether females perform more courtship displays towards larger males and whether females allocate their reproductive effort depending on the size of their mate by experimentally assigning females to either large or small males. I found that females displayed more towards larger males, thereby suggesting a female preference for larger males. Further, females produced heavier eggs and heavier clutches but not more eggs when paired with large males. My experiments show that females in this species adjust their offspring weight and, thus, presumably offspring quality according to the size of their mate.     

Apogon smithi (Kotthaus, 1970) (Teleostei: Apogonidae), a Red Sea cardinalfish colonizing the Mediterranean Sea

Smith's cardinalfish Apogon smithi is recorded for the first time in the Mediterranean Sea. Six specimens were caught by commercial trawler north of Jaffa, Israel, at depths of 40 m and the relatively high number of specimens suggests that A. smithi has established a sustainable population. This is the third Indo-Pacific apogonid species documented in the Mediterranean Sea, and is assumed to be a migrant originating from the Red Sea.     

Extra‐pair mating in a socially monogamous and paternal mouth‐brooding cardinalfish

Many vertebrates form monogamous pairs to mate and care for their offspring. However, genetic tools have increasingly shown that offspring often arise from matings outside of the monogamous pair bond. Social monogamy is relatively common in coral reef fishes, but there have been few studies that have confirmed monogamy or extra‐pair reproduction, either for males or for females. Here, long‐term observations and genetic tools were applied to examine the parentage of embryos in a paternally mouth‐brooding cardinalfish, Sphaeramia nematoptera. Paternal care in fishes, such as mouth‐brooding, is thought to be associated with a high degree of confidence in paternity. Two years of observations confirmed that S. nematoptera form long‐term pair bonds within larger groups. However, genetic parentage revealed extra‐pair mating by both sexes. Of 105 broods analysed from 64 males, 30.1% were mothered by a female that was not the partner and 11.5% of broods included eggs from two females. Despite the high paternal investment associated with mouth‐brooding, 7.6% of broods were fertilized by two males. Extra‐pair matings appeared to be opportunistic encounters with individuals from outside the immediate group. We argue that while pair formation contributes to group cohesion, both males and females can maximize lifetime reproductive success by taking advantage of extra‐pair mating opportunities.     

Sexual selection and the evolution of exclusive paternal care in arthropods

Internal fertilization and anisogamy are thought to impede the evolution of exclusive paternal care by reducing paternity assurance and increasing male promiscuity. The potential role of sexual selection in easing these constraints is currently being examined in vertebrates but has not been seriously studied in most arthropods. To distinguish the effects of sexual from natural selection on the evolution of arthropod paternal care, I tested predictions of the state of several life history and behavioural traits under both forms of selection across all known taxa with exclusive paternal care. The results suggest parallels between prezygotic nuptial gifts and exclusive postzygotic paternal care and support the hypothesis that, in arthropods, male behaviours that enhance female reproductive success either directly by releasing females from the fecundity constraints of maternal care (enhanced fecundity hypothesis) or indirectly by identifying mates with superior genes (handicap principle) are traits on which sexual selection has acted. Under such conditions males willing to guard young become preferred mates for gravid females and enjoy greater promiscuity than males unable or unwilling to guard. Females use nest construction or the act of guarding another female's eggs as honest signals of paternal intent and quality. Copyright 2000 The Association for the Study of Animal Behaviour.