Egg mass destroying and guarding behaviour of the giant water bug,Lethocerus deyrollei Vuillefroy (Heteroptera: Belostomatidae)

Egg mass destroying behaviour of femaleLethocerus deyrollei and male defending behaviour were observed in a densely vegetated concrete pond. In 3 of 9 cases of male-female interactions, the males successfully guarded their egg masses. In 4 of the 6 remaining cases in which the egg masses were destroyed by the female, females successfully took over the mate and laid their own egg masses the same night. These results suggest that male brooding guards the egg mass from females, as well as supplying eggs with water.     

Male body size and brooding success under natural conditions in the freshwater Japanese goby, Rhinogobius sp. OR (orange type)

Males of the Japanese goby Rhinogobius sp. OR (orange type) establish nests under stones in streams. They provide care to egg masses until hatching. We carried out field observations and a field experiment in a natural stream to examine the effect of male body size on brooding success. An experiment excluding guarding males indicated that their presence has a positive effect on nest defense. Field data showed that male body size was positively correlated with the size of the egg mass that was initially found at the nest. Furthermore, a sequential increase in egg mass size seen in the nests of larger males indicated that multiple females spawned during a single breeding cycle of larger males. To examine male brooding success, two dependent variables, egg mass persistence (days from initial egg mass to disappearance or hatching) and hatching success were analyzed. The results indicated that the variation found in both dependent variables was significantly explained by two independent variables, namely, initial egg-mass size and the number of matings. It is also suggested that male body size indirectly influenced brooding success through positive correlations with these independent variables.     

Egg mass destroying behaviour of the female giant water bugLethocerus deyrollei Vuillefroy (Heteroptera: Belostomatidae)

After being laid on emergent aquatic vegetation, the egg masses ofLethocerus deyrollei are brooded by the male. In laboratory studies, females were observed to destroy egg masses and ingest the fluid of eggs. Brooding males fought with these attackers at first, but then gave up the defense and mated with them. After destroying the egg masses, females laid new ones at the same sites on the same night or the following one, and males brooded the new offspring. The population density of this species is very low. Most males engage in brooding and cease to become acceptable mates after most of the females lay the first egg masses. It is costly for females to search out free males in the aquatic vegetation. By destroying egg masses, however, individual females can gain new mates with little exertion and can make them brood their own offspring. Furthermore, the survival of their own offspring increases with the elimination of their competitors.     

Exclusive Male Egg Care and Determinants of Brooding Success in a Millipede

The evolution of exclusive male parental care is a major and controversial issue in behavioural ecology. Although arthropods practicing paternal care are thought to be key taxa for investigating this issue, few studies have attempted to clarify the selection factors associated with male behaviour and fitness consequences in arthropods. In the millipede Brachycybe nodulosa, males curl their bodies around egg masses on the undersides of decaying logs. Male‐removal experiments in the laboratory strongly suggest that males defend the eggs against fungal infection. Orphaned eggs were soon covered by hyphae and no eggs hatched, whereas almost all eggs brooded by males successfully hatched. The egg‐brooding males showed no aggressive responses when disturbed. Only some mature males bred in the field. Furthermore, the number of eggs brooded varied greatly among the males. Selected generalized linear models revealed that males with a wide seventh body segment, which possesses gonopods (genital legs), tended to succeed in brooding; and males with a wider body also obtained more eggs. Colony attributes had no significant effects on male brooding. We discuss the possible sexual selection mechanisms that could accomplish this pattern of brooding success among male B. nodulosa.     

Paternal care behaviour of the giant water bug Kirkaldyia deyrolli (Heteroptera: Belostomatidae) against ants

1. Although potentially vulnerable to predators, the offspring of subsocial insects are effectively protected by their parent(s). The female giant water bug Kirkaldyia deyrolli lays its egg masses on the vegetation above the water surface in aquatic environments and the males supply the eggs with water and guard them against cannibalistic females until hatchling dispersal. Field observations showed that egg masses are attacked by ants if the attending males are not present. 2. Laboratory experiments were conducted to evaluate the effects of paternal care by K. deyrolli against the ant Tetramorium tsushimae by means of four treatments: attending male with ant approach (WM‐WA); no attending male with ant approach (NoM‐WA); attending male without ant approach (WM‐NoA); and no attending male without ant approach (NoM‐NoA). 3. The rate of offspring survival was lower in the NoM‐WA group (45.3%) than in any other group, which showed similar offspring survival (WM‐WA = 80.4%, WM‐NoA = 75.1%, NoM‐NoA = 80.3%). Moreover, there were a total of 44 interactions between the attending male and ants in WM‐WA, and of these, a chemical compound was released by the attending male four times; this probably deterred ants from attacking because the ants went back to their colony. 4. In conclusion, the attending male can protect its eggs from ant predators and its care has an important role. To the best of the authors' knowledge, this is the first report of Lethocerinae males protecting their egg masses from ants by means of physical and chemical defence.     

The polygamous mating system of the sea spider Achelia simplissima

Most species of pycnogonids are sexually dimorphic and all have exclusive male care of the offspring, characteristics that make them essential for studies on sex-roles, sexual selection, and parental investment. However, sea spiders have been understudied because of their small size, cryptic coloration, and often patchy distribution, and little is known about their courtship and mating behaviors. The mating habits of both male and female Achelia simplissima (Hilton 1939) were studied experimentally and observationally. This species mates year-round and females commonly initiate courtship by actively ‘pumping’ their bodies near a male. When both nonparental and parental males were present, females mated significantly more often with males that were not carrying egg masses. Each mating event resulted in a single egg mass. Most often, males placed the first egg mass on their right oviger and then alternated between ovigers with subsequent matings. The newest (least developed) egg mass was always placed at the tip of the oviger. Both males and females routinely mated multiple times and had multiple mates; in the field, males were found carrying up to twelve egg masses simultaneously. This is the first experimental study to describe both the male and female mating system of a pycnogonid, and the first observations of courtship and mating for any species with the ammotheid type of ovigers.     

Brochosome influence on parasitisation efficiency of Homalodisca coagulata (Say) (Hemiptera: Cicadellidae) egg masses by Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae)

Abstract. 1. Many cicadellid females in the tribe Proconiini (Hemiptera: Cicadellidae) cover their egg masses with specialised, usually rod‐shaped, brochosomes as the eggs are being laid. The brochosomes are produced in Golgi complexes in the Malpighian tubules of Cicadellidae. In contrast to the gravid females, adult males, pre‐reproductive adult females, and nymphal males and females produce specialised, usually spherically shaped brochosomes. Brochosomes are also used to cover the external surfaces of nymphs and newly moulted adult males and females. 2. The function of the brochosome covering the egg masses is unknown but various hypotheses have been suggested, including protecting the eggs against pathogens, predators, and parasitoids. Based on preliminary observations of Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae) parasitising the eggs of the cicadellid, Homalodisca coagulata (Say), it is speculated here that brochosomes covering an egg mass hinder parasitisation of eggs by G. ashmeadi. This hypothesis was tested by observing G. ashmeadi females foraging on leaves with H. coagulata egg masses heavily covered with rod‐shaped brochosomes vs. those lacking brochosomes. 3. Cox's proportional hazards model was used to evaluate the probability, per unit time, that a female G. ashmeadi displayed the sequence of behaviours that ended in successful oviposition as influenced by five variables: (a) presence or absence of brochosomes on an egg mass, (b) the leaf surface, upper or lower, being searched by the parasitoid (the egg masses are laid in the parenchyma on the lower leaf surface), (c) the parasitoid's previous ovipositional experience, (d) egg mass size, and (e) the parasitoid's age. 4. Brochosomes significantly decreased oviposition efficacy of G. ashmeadi females. Scanning electron microscopy showed that females exposed to brochosome‐covered egg masses had brochosomes adhering to their tarsi, legs, antennae, and eyes, all of which prompted extensive bouts of grooming.     

Postural Shifts During Egg‐Brooding and Their Impact on Egg Water Balance in Children’s Pythons (Antaresia childreni)

Parental care typically consists of distinct behavioral components that are balanced to address the multiple needs of offspring. Female pythons exhibit post‐oviposition parental care in which they coil around their parchment‐shelled eggs throughout incubation (40–80 d). Subtle postural shifts during egg‐brooding facilitate embryonic gas exchange but may entail hydric costs to the clutch. This study used a simple behavioral model to (1) further quantify the costs and benefits of specific parental behaviors to developing offspring and (2) determine the influence that developmental stage and relative clutch mass have on parental behavior. Although previous research has demonstrated that egg‐brooding as a whole reduces clutch water loss, we hypothesized that egg‐brooding female pythons specifically adopt a tightly coiled posture to conserve embryonic water, but must make postural adjustments to enhance gas exchange between the clutch and nest environments at the cost of increased clutch water loss. We measured rates of water loss in brooding Children’s pythons (Antaresia childreni) and their respective clutches (i.e., brooding units) and monitored changes in brooding posture. We conducted serial trials to elucidate the effect of developmental stage on postural adjustments and water loss. Results demonstrated that the proportion of time females spent in a tightly coiled posture was inversely related to mean water loss from the brooding unit. Analyses indicated that slight adjustments in posture led to bursts in brooding unit water loss. Indeed, brooding unit water loss during postural adjustments was significantly higher than during tight coiling. These findings imply that python egg‐brooding provides an adjustable diffusive barrier that leads to discontinuous gas exchange, which minimizes clutch water loss. Because females with larger relative clutch masses spent more time tightly coiled, egg‐brooding female pythons may use a ‘water first’ strategy in which they intentionally conserve clutch water at the cost of reduced embryonic respiratory gas exchange.     

Determinants of male mating success in a natural population of a stream goby of the genus Rhinogobius

The mating success of individually identified males of a stream goby, Rhinogobius sp. CB (cross‐band type), was recorded over one breeding season. One to 3 year‐old males were active in mating, but 3 year‐old males, which accounted for 36% of the population, amounted to c . 70% of the total males guarding eggs in the nest. Three quarters of the breeding males had only one brooding cycle, but the others had two or three. All the latter males changed their nest sites between cycles within a riffle. In 1 and 2 year‐old males, the number of brooding cycles contributed more to the mating success than egg mass size in one brooding cycle. For mating success of 3 year‐old males, the egg mass size in one brooding cycle, which can be enhanced by spawning with a large female or multiple females, was as important as the number of brooding cycles. These male reproductive tactics could be attributed to the age‐related ability of nest construction and mate acquisition.     

Sexual attractiveness shared by both sexes mediates same‐sex sexual behaviour in the parasitoid wasp Telenomus triptus

The mating behaviour of a quasi‐gregarious egg parasitoid Telenomus triptus Nixon (Hymenoptera: Platygastridae), which exploits egg masses of a stink bug Piezodorus hybneri (Heteroptera: Pentatomidae), is examined in the laboratory. In this parasitoid wasp, male adults that emerge earlier stay at the natal egg mass and mate with subsequently emerging females. In the present study, a male adult that encounters the emergence of another male always waits for it to egress, and then mounts the newly emerging male. To examine why males of T. triptus show same‐sex sexual behaviour, male adults are presented with a parasitized host egg mass or a freshly killed wasp. Male adults are observed to remain at host egg masses from which only male wasp(s) had emerged. In addition, male adults attempt to copulate with freshly killed young male wasps. It is suggested that newly emerging male wasps are targets of same‐sex sexual behaviour because they possess cues for male sexual behaviour similar to the cues of females. Both the sex and age of freshly killed wasps affect the frequency of the sexual behaviour of male adults: females are more attractive than males, although their attractiveness declines with age. When the mating opportunity is restricted to the natal egg mass, the costs of failing to notice newly emerging female adults should be extremely high. Therefore, males are forced not to discriminate the sex, resulting in same‐sex sexual behaviour.     

Spawning and biparental egg-care in a temperate filefish,Paramonacanthus japonicus (Monacanthidae)

Synopsis Reproductive habits of a temperate filefish, Paramonacanthus japonicus, were studied on a rocky reef at Tsuyazaki, Fukuoka, Japan, from 1989 through 1990. Males had territories of 30–70m² and defended them from conspecific males and potential egg predators such as another filefish, Stephanolepis cirrhifer. Egg masses were found on the sandy bottom in male territories. Individual discrimination of males and females occurring in three male territories revealed that males and females stayed in stable pairs during one month of observation in 1989. In these stable pairs, males fed only within their territories, but females occasionally foraged outside. The occurrence of egg masses within male territories and biparental egg care showed that fish were reproducing as monogamous pairs. Contrary to this, males tagged in 1990 changed their territories after the disappearance of females, and males and females mated polygamously. Spawning was observed only four times during the study period, between 1633 and 1754h. Prior to spawning, the female prepared a spawning bed on the sandy bottom. The male nuzzled the female and the pair spawned, touching their gonopores on the spawning bed. Spawning was very quick and took only 1–3 seconds. The adhesive eggs were spherical with a diameter of 0.56 mm. They were mixed with sand particles and formed a doughnut-shaped mass of about 4 cm in diameter. One egg mass contained 3300–3800 embryos of similar developmental stage, which hatched 2–3 days later. P. japonicus appears to be monogamous but may also practice polygamy when pair-bonds are unstable.     

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.     

Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth‐brooding cichlid Ophthalmotilapia ventralis

A rare form of alternative reproductive behaviour without simultaneous parasitic spawning was observed in Ophthalmotilapia ventralis, a lekking mouth‐brooding cichlid from Lake Tanganyika. Floater males attempted to sneak opportunistically into the territory to actively court the female, while the owner (bourgeois male) defended the territory against other potential intruders. Floater males had more body fat than territory owners and generally higher condition factors. In field experiments, the response of bourgeois males and courted females was tested towards floaters and egg predators (a catfish Synodontis multipunctatus) present in the territories. Territory owners responded aggressively particularly to floaters, and female responsiveness to bourgeois male courtship tended to decline when floaters were present. The potential influence of reproductive parasitism on sexual selection in mouth‐brooding cichlids is discussed.     

Paternity analysis in an egg‐carrying aquatic insect Appasus major (Hemiptera: Belostomatidae) using microsatellite DNA markers

The giant water bug Appasus major exhibits a peculiar reproductive behavior where females lay eggs on the backs of males. A male and female pair performs frequent repeat copulations during the oviposition behavior, and the male carries the deposited eggs until hatching. Such characteristic behaviors predict that the eggs are fertilized by the brooding males. If males carry eggs of other unrelated males, the egg carrying will drastically decrease the fitness of the carriers. In this study, we examined genetic relationships between the 489 eggs and nine males carrying them collected from the field, using microsatellite DNA markers. We revealed that in total, 28.4% of the eggs were of other male origin. This is the first report of frequent brood parasitism in an aquatic egg‐carrying hemipteran insect. The brood parasitism is adaptive for the females probably because it enables them to increase the chance of oviposition, or it can equalize motility risk of the eggs of each mate.     

Male brooding behaviour of the giant water bugLethocerus deyrollei vuillefroy (Hemiptera: Belostomatidae)

The male brooding behaviour ofLethocerus deyrollei was investigated. Eggs were laid as masses on sticks above the water surface. Males did not leave the sticks until the eggs hatched. They mainly stayed at the bases of the sticks in water in the day, and frequently climbed up at night covering the egg-masses with their bodies. Eggs with male brooding had a 94.3% hatching rate. Eggs without male brooding failed to hatch and desiccated. Eggs with brooding considerably increased in wet weight in development; eggs without brooding decreased in wet weight. Eggs without male brooding and artificially supplied with water had a 93.2% hatching rate. Male brooding is considered to supply eggs with water.     

Brood protection at a cost: mouth brooding under hypoxia in an African cichlid

This study quantifies the behavioral response of the widespread mouth brooding African cichlid Pseudocrenilabrus multicolor victoriae to progressive hypoxia. We exposed four gender/stage classes of P. multicolor (males, brooding females, females that had just released young, and non-brooding females) to progressive hypoxia and recorded the percent time spent using aquatic surface respiration (surface skimming, ASR) and gill ventilation rates. This was done for fish collected from three sites in Uganda (lake, swamp, and river) after long-term acclimation to normoxia. There was no effect of site of origin on response to hypoxia, but ASR thresholds did differ between gender/stage classes. The oxygen level (threshold) at which spent 10, 50, and 90% of their time at the surface using ASR was much higher for brooding females than for males, whereas ASR thresholds did not differ between non-brooding females and males. Similarly, the level at which ASR was initiated was much higher in brooding females than males, but did not differ between males and non-brooders, or between males and females than had just released young. The rate of gill ventilation dropped significantly in males and all stages of females after initiation of ASR, suggesting that surface skimming increases efficiency of oxygen acquisition. These results suggest that mouth brooding in female P. multicolor ASR improves oxygen uptake but imposes a cost in terms of time spent at the water surface, and this may affect maternal predation risk in low-oxygen habitats.     

Egg attendance and brooding by males of the giant water bugLethocerus medius (Guerin) in the field (Heteroptera: Belostomatidae)

Males of the giant water bug Lethocerus medius(Guerin) typify their monobasic subfamily, the Lethocerinae, in that they do not brood eggs attached to their backs as do males of all members of the subfamily Belostomatinae. Exclusive male parental investment as expressed in the Belostomatinae is extremely rare behavior among animals, and evolution of the trait is obscure. Lethocerus mediusmales apparently remain with their mates through oviposition and are consistently found in attendance of eggs after the female has departed. This behavior may enhance paternity assurance at no cost in opportunity for polygyny. Two double clutches of eggs were found, from which we infer the potential for polygynous matings and shared parental investment. Male L. mediusbrood attended egg clutches above the surface of the water, where they may moisten them, shade them, and defend them against predation. Egg attendance/brooding by L. mediusand other Lethocerusspecies may represent a plesiomorphic state from which paternal back- brooding evolved in the Belostomatinae.     

Double brooding and offspring desertion in the barn owl Tyto alba

Many bird species produce two annual broods during a single breeding season. However, not all individuals reproduce twice in the same year suggesting that double brooding is condition‐dependent. In contrast to most raptors and owls, the barn owl Tyto alba produces two annual clutches in most worldwide distributed populations. Nevertheless, the determinants of double brooding are still poorly studied. We performed such a study in a Swiss barn owl population monitored between 1990 and 2014. The annual frequency of double brooding varied from 0 to 14% for males and 0 to 59% for females. The likelihood of double brooding was higher when individuals initiated their first clutch early rather than late in the season and when males had few rather than many offspring at the first nest. Despite the reproductive benefits of double brooding (single‐ and double‐brooded individuals produced 3.97 ± 0.11 and 7.07 ± 0.24 fledglings, respectively), double brooding appears to be traded off against offspring quality because at the first nest double‐brooded males produced poorer quality offspring than single‐brooded males. This might explain why females desert their first mate to produce a second brood with another male without jeopardizing reproductive success at the first nest. Furthermore, the reproductive cycle being very long in the barn owl (120 d from start of laying to offspring independence), selection may have favoured behaviours that accelerate the initiation of a second annual brood. Accordingly, half of the double‐brooded females abandoned their young offspring to look for a new partner in order to initiate the second breeding attempt, 9.48 d earlier than when producing the second brood with the same partner. We conclude that male and female barn owls adopt different reproductive strategies. Females have more opportunities to reproduce twice in a single season than males because mothers are not strictly required during the entire rearing period in contrast to fathers. A high proportion of male floaters may also encourage females to desert their first brood to re‐nest with a new male who is free of parental care duties.     

Endocrine correlates of parental care in an Antarctic winter breeding seabird, the emperor penguin, Aptenodytes forsteri

Plasma levels of luteinizing hormone (LH) and prolactin associated with parental behavior were measured in the Antarctic winter breeding emperor penguin, Aptenodytes forsteri. Males exclusively incubate the egg while females exclusively brood the nonhomeothermic young; both sexes alternate in rearing the homeothermic young. Birds were sampled on arrival from the sea through egg laying, incubation, and brooding. All parent birds lost their chicks at the end of the brooding period due to harsh weather but sampling continued. In females, LH titers dropped after egg laying but levels were restored when the birds returned from the sea to brood the chicks and were not depressed by high prolactin levels. Plasma prolactin remained low in males captured on arrival and kept until the free-living males finished incubation. In breeders, prolactin secretion increased during the prelaying period when day length decreased. Prolactin levels stayed elevated in males during incubation and in brooding females returning after a 2-month absence at sea. Prolactin values were higher in brooding females than in males ending incubation or returning in late brooding. These levels did not drop after chick loss, and the sexual difference in prolactin values was maintained after breeding failure. In emperor penguins, increased prolactin secretion appears to be triggered around the time of egg laying and continues, driven by an endogenous mechanism, through incubation and brooding until rearing is completed. Prolactin secretion independent of external stimuli may have evolved in pelagic seabirds to maintain parental care despite long absences at sea from the breeding colony.     

Male mating success and female mate choice in the river sculpin,Cottus nozawae (Cottidae)

Synopsis Mating success of males and its correlates were investigated in a natural population of the polygynous fluvial sculpinCottus nozawae. Furthermore, the female mate preference of this species was examined experimentally under alternative conditions for mating in a stream. The mating success of individual males (the number of females with which a male mated) ranged between 0 and 8 with a mean of 2.41 in 1983 and 2.52 in 1989, in a population of which the sex ratio was about 1 : 2 in both years, skewed toward females. Mainly due to the excess of nests without egg masses and the few nests with one egg mass, the distribution of male mating success did not fit a Poisson distribution, indicating its non-randomness. Male mating success was not correlated either with the size of the nest rocks or with the male size, suggesting that these two variables are not determinants of mating success. The mate choice experiments demonstrated that females of this species more frequently chose smaller males as mates whose nests already contained eggs than large males without eggs. Additionally, an analysis of stomach contents of guarding males suggested that the parental males ate their own eggs during egg guarding (filial-cannibalism). Based on these results and on a comparison of reproductive characteristics with congeneric species, it is suggested that one of the most important determinants for female mate choice inCottus species may be whether or not parental males are filial egg cannibals.