Spawning behavior of Arctic charr (Salvelinus alpinus): Spawning synchrony,vibrational communication,and mate guarding

A mismatch in synchrony between male and female gamete release in external fertilizers can result in reduced or failed fertilization, sperm competition, and reduced paternity. In Arctic charr (Salvelinus alpinus), males can adopt either a guard or sneak tactic resulting in both pre‐ and postcopulatory competition between males with alternative reproduction tactics. Here, spawning behavior of free‐living Arctic charr was video‐recorded, and their reproductive behavior was analyzed. From evaluating 157 spawning events, we observed that females mainly spawned with a guarding male and that the female and the guarding male synchronized timing of gamete release under sperm competition. Although sneakers spawned with higher synchrony than the guarding male in single‐male spawning events, the average sneaker released his milt less synchronized with the female than the guarding male under sperm competition. Approximately 50% of the recorded spawning events occurred under sperm competition, where each event included an average of 2.7 males. Additionally, sneakers were more exposed to sperm competition than guarding males. An influx of males, in close proximity to the female, occurred during the behavioral sequences leading up to egg release, but this influx seemed not dependent on egg release, suggesting that something else than gonadal product attracts sneaker males to the spawning female. Just before and during the actual release of gametes, the spawning couple vibrates their bodies in close contact and it seems likely that this vibrational communication between the spawning couple, which results in a larger amplitude sound wave than seen under regular courting, reveals time of gamete release to sneaker males. Thus, vibrational communication may enable synchrony between the guarding male and the female, and this might be traded against the cost of higher detectability from surrounding sneaker males, eavesdropping in close proximity.     

A Test for Male Parental Care in a Fundulid, the Bluefin Killifish, Lucania goodei

Under field conditions, breeding male bluefin killifish, Lucania goodei, have been observed aggressively defending territories from other breeding males, non-breeding females, and minnows (mainly Notropis harperi). We performed an aquarium experiment to test whether male aggression serves to protect newly deposited eggs from predation. We allowed a male and a female to spawn in a yarn mop, removed the female, and exposed the eggs to one of four treatments (spawning male present, two minnows present, spawning mal+two minnows present, no adult fish present). Mops were censused daily for seven days. Egg predation rates were highest in the male+minnows and male only treatments. Egg predation rates in the male+minnows treatment did not differ from the predicted predation rate (sum of male only and minnows only treatments). Hence, there is no evidence for male parental care in L. goodei. In addition, we compared the egg predation rates (filial cannibalism) between males of 3 different color morphs and found no evidence for differential egg cannibalism.     

Sex-biased egg cannibalism in spawning walleye pollock: the role of reproductive behavior

We studied inadvertent egg cannibalism in spawning stocks of walleye pollock, Theragra chalcogramma, in the Gulf of Alaska and the Bering Sea between 1986 and 1996. Male pollock had on average 3 times more eggs in their stomachs than females. For both sexes adult fish of average body length had more eggs in their stomach than did smaller or larger fish. When maturity of fish was taken into account, actively spawning males had the highest numbers of eggs in their stomachs. We found weak evidence for a diel variation; the number of eggs per stomach was high in both sexes during the day and lower during the night. We suggest two possible explanations for this phenomenon. Sex-biased egg cannibalism may reflect the differential time spent in layers of high egg densities. Hydroacoustic and trawl catch data from both areas suggest that males aggregate deeper than females. Spawning takes place in the deeper layers of the fish aggregation, so males spend more time in high egg densities. Alternatively, males may be more active than females and increased gill ventilation and/or drinking rates may be responsible for the differences in egg cannibalism.     

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.     

Sperm and milt characteristics and male v. female gametic investment in the Caribbean reef fish, Thalassoma bifasciatum

Individual sperm cells produced by two male morphs of the bluehead wrasse Thalassoma bifasciatum did not differ in size (i.e. cell volume). Initial phase (IP) males (high sperm competition) had a 60% higher sperm concentration in their milt than did terminal phase (TP) males (low sperm competition), which may reflect differences in how accurately the two male morphs need to allocate sperm to their spawns. The energy density of milt was about 16% lower than that of eggs. Estimates of gametic energy investment based on (a) the difference in testis weights between the beginning and the end of the spawning period and (b) the number of sperm released in natural spawns (determined in other studies), suggested that, on a daily basis, IP males invest about 65% of that of females. Estimates based on stripping milt from IP males at the beginning and the end of the spawning period, however, indicated that their daily energy investment in gamete production is about 10% of that of females Gametic investment by TP males is lower than that by both IP males and females.     

Egg cannibalism in Barents Sea capelin in relation to a narrow spawning distribution

The spawning distribution of Barents Sea capelin Mallotus villosus off northern Norway in 2002 was restricted to a narrow area at the easternmost spawning grounds. There was an increase in abundance and a marked shift in aggregation area from east towards west during 11 March to 4 April, as the capelin went from prespawning through spawning to spent stages. The capelin stomachs were either empty or contained capelin eggs, often mixed with sand. Both the occurrence of cannibals and stomach fullness increased with stage of maturity, being highest in spent fish, and higher in males than in females. No differences were found between cannibals and non-cannibals of the same sex when adjusted for total length ( L _T), age, L _T at age and condition factor. At similar stomach fullness, the females had consumed more eggs than the males. This was attributed to a higher proportion of empty and broken eggs and less sand in females compared to males. In the full stomachs, the mean consumption in females and males was 623 and 334 eggs, respectively, whereas the respective maximum egg consumption was 871 and 683 eggs. The minimum estimates (given no digestion) of mean ± 95% CL egg consumption in spent females and males were 75·4 ± 6·9 and 58·4 ± 12·0 eggs, respectively, implying a minimum mortality of 1–2% of the total egg production caused by cannibalism.     

Experimental evidence for paternal effects on offspring growth rate in Arctic charr (Salvelinus alpinus)

Sexual selection theory predicts that females should choose males that signal viability and quality. However, few studies have found fitness benefits among females mating with highly ornamented males. Here, we use Arctic charr (Salvelinus alpinus), a teleost fish with no parental care, to investigate whether females could gain fitness benefits by mating with highly ornamented and large-sized males. Carotenoid-based coloration signalled by males during spawning is believed to be an indicator of good genes for this species. Paternal effects on offspring size (body length and dry body mass) were examined experimentally by crossing eggs and sperm in vitro from 12 females and 24 males in a split-brood design and raising larvae to 30 days past hatching. We clearly demonstrated that there was a relationship between offspring size and paternal coloration. However, a negative interaction between paternal length and coloration was evident for offspring length, indicating that positive effects of paternal coloration were only present for smaller males. Thus, the red spawning coloration of the male Arctic charr seems to be an indicator of good genes, but the effect of paternal coloration on offspring length, an indicator of 'offspring quality', is size dependent.     

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.     

Dummy Egg Production by Female Cardinalfish to Deceive Cannibalistic Males: Oogenesis without Vitellogenesis

Filial cannibalism occurs in a variety of taxa, especially in fish exhibit paternal care. In the Apogonidae, males mouthbrood a cohesive mass of eggs received from a single female, although the males frequently eat the entire brood. It has been recognized that a primary factor concerning entire brood cannibalism is the brood size produced by females, as the parent eats a small egg mass so long as the reproductive return does not exceed the cost of providing care. In Apogon lineatus, approximately 18% of each brood was occupied by abnormal eggs lacking yolk, which were hydrated without the vitellogenesis phase and eventually ovulated with other normal eggs as a single egg mass. By not providing yolk to some eggs within the brood, A. lineatus females may succeed in producing an apparently large brood, reducing the likelihood of entire brood cannibalism by males.     

Parental fish change their cannibalistic behaviour in response to the cost-to-benefit ratio of parental care

Partial filial cannibalism, the act of cannibalizing some offspring, has been explained as a response to the high energetic cost of care. I tested this hypothesis by manipulating the cost-to-benefit ratio of care in the scissortail sergeant, Abudefduf sexfasciatus, a tropical damselfish with male care. Background egg mortality was lower than the incidence of cannibalism, confirming that males did not just dispose of dead eggs. Investment in the current brood affected future investment, because males forced to skip a brood cycle put more effort into courtship during the following cycle and obtained larger broods than did unmanipulated males. Any factor influencing the cost-to-benefit ratio of parental care should also affect the incidence of cannibalism. I reduced the cost of care by supplementary feeding and reduced the benefit of care by simulating a decrease in paternity certainty through simulated intrusions by non-nesting males. Supplementary feeding significantly reduced partial filial cannibalism by parental males, a result compatible with the hypothesis that eggs are consumed to cover the energetic costs of parental care. Cannibalism decreased regardless of whether males were fed with conspecific eggs or crabmeat. Cannibalism was only reduced but not fully eliminated by supplementary feeding, and residual levels of cannibalism after feeding were similar to the background rate of egg mortality. Simulated intrusions by non-nesting males led to an increase in filial cannibalism and a decrease in parental effort.     

Filial cannibalism in an assassin bug

Filial cannibalism has been described in many fish species with male parental care, and has typically been explained as a response to high energetic costs of brood defence and decreased feeding opportunities during the period of care. We investigated filial cannibalism in an insect, the assassin bug Rhinocoris tristis. In this species, males guard eggs of a number of females, cannibalizing some of their offspring within the brood. We monitored guarding males in both the field and the laboratory. Males typically ate eggs around the periphery of the brood, which were those most likely to have been parasitized by wasps. However, cannibalism persisted in the laboratory in the absence of parasites, and the number of cannibalized eggs was related to the length of care and overall brood size, suggesting that males use eggs as an alternative source of food. This conclusion was further supported by the fact that males in the field did not lose weight while guarding, despite being unable to forage efficiently while caring. Males were also observed to adopt broods, but in a laboratory experiment did not eat more eggs from adopted than from their own broods.     

The evolution of filial cannibalism and female mate choice strategies as resolutions to sexual conflict in fishes

Filial cannibalism (the consumption of one's own viable offspring) is common among fish with paternal care. In this study, I use a computer simulation to study simultaneous evolution of male filial cannibalism and female mate choice. Under certain conditions, selection on parental males favors filial cannibalism. When filial cannibalism increases a male's probability to raise the current brood successfully, filial cannibalism also benefits the female. However, when egg eating is a male investment into future reproduction, a conflict between female and male interests emerges. Here I investigate how female discrimination against filial cannibals affects evolution of filial cannibalism and how different female choice criteria perform against filial cannibalism. The introduction of discriminating females makes the fixation of filial cannibalism less likely. I introduced three different female choice criteria: (1) females who could discern a male's genotype, that is, whether the male was going to eat eggs as an investment in future reproductive events; (2) energy-choosing females that preferred to mate with males who had enough energy reserves to live through the current brood cycle without consuming eggs; and (3) females that preferred to mate with already mated males, that is, males with eggs in their nest. Genotype choice never coexisted with filial cannibals at fixation and filial cannibals were unable to invade a population with genotype-choosing females. Energy choice was successful only when males had high energy reserves and were less dependent on filial cannibalism as an alternative energy source. The egg choosers frequently coexisted with the cannibals at fixation. When the female strategies were entered simultaneously, the most frequent outcome for low mate sampling costs was that both the cannibals and the egg choice was fixed and all other strategies went extinct. These results suggest that sexual conflicts may not always evolve toward a resolution of the conflict, but sometimes the stable state retains the conflict. In the present case, this was because the egg-preference strategy had a higher fitness than the other female strategies. The outcome of this simulation is similar to empirical findings. In fish with paternal care, male filial cannibalism and female preference for mates with eggs commonly co-occur.     

Herring as cannibals

Egg cannibalism near the sea bottom was observed in herring Clupea harengus at the end of the spawning season. About 10% of the individuals had consumed eggs and egg feeders were predominantly spent males.     

Stress reduces the quality of gametes produced by rainbow trout.

In this study we have used the rainbow trout as a model animal to study the biological consequences of stress in terms of gamete quality and quantity. Groups of 30 mature male and female rainbow trout were subjected to repeated acute stress during the 9 mo prior to spawning. Time of ovulation, fecundity, and egg size were recorded in mature females, and sperm counts were carried out on the milt from the male fish, from both the stressed and control groups. Eggs from ovulated females were fertilized with milt from males subjected to the same treatment regime. Approximately 300 eggs from each female were fertilized with a sperm dilution of 10(-3) in diluent. Subsequent development of the fertilized eggs was then monitored. There were no differences in somatic weight or length between the two groups at the end of the experiment, but exposure of rainbow trout to repeated acute stress during reproductive development resulted in a significant delay in ovulation and reduced egg size in females, significantly lower sperm counts in males, and, perhaps most importantly, significantly lower survival rates for progeny from stressed fish compared to progeny from unstressed control fish. Hence, stress reduces the quality of gametes produced by rainbow trout.     

Cannibalism on eggs by dark chub, Zacco temmincki (Temminck & Schlegel) (Cyprinidae)

During spawning male dark chub, Zacco temmincki (Temminck & Schlegel), buried eggs by stirring up the river bed with their anal fins. No parental care was shown for eggs after spawning. Many satellites (both males and females) preyed upon eggs at the instant of spawning. The number of eggs produced is a function of body length [log₁₀ E =−0.273+3.519log₁₀ S , where E is the number of eggs and S is standard length (cm)]. From the size distribution of females that spawned during a reproductive season, the total number of spawning sites used and mean number of eggs per spawning site, at least 97.1% eggs were estimated to be consumed by cannibalism. This marked cannibalism resulted from a lack of parental care and the presence of many satellites produced by the polygynous mating system.     

Cuckoldry incites cannibalism: male fish turn to cannibalism when perceived certainty of paternity decreases

Perceived certainty of paternity is expected to influence a male's behavior toward his offspring: if he is uncertain of his reproductive success with a current brood due to the presence of cuckolders, it may benefit him to invest instead in future reproduction. A decrease in perceived certainty of paternity incites filial cannibalism (the eating of one's own offspring) in some teleost fishes that provide parental care; however, no work has demonstrated that cannibalism increases proportionately with increased levels of cuckoldry. Here we show for the first time in a fish with no parental care that as the number of cuckolders at a spawning event increases, so does the probability that a male will cannibalize eggs. In field observations of Telmatherina sarasinorum, a small fish endemic to Sulawesi, Indonesia, males increased filial cannibalism behavior threefold in the presence of one cuckolder and nearly sixfold in the presence of two or more cuckolders. This suggests that males may use detection of cuckolders as an indication that the paternity of current offspring has been compromised.     

Mating behavior in the black hamlet — gamete trading or egg trading?

Synopsis The black hamlet (Hypoplectrus nigricans, Serranidae) is a simultaneous hermaphrodite, like many other serranines. It has external fertilization and planktonic eggs and engages in a kind of reciprocal spawning consisting of three components: (1) The clutch is divided into sequentially spawned parcels. (2) Partners regularly alternate release of parcels in a spawning bout. (3) Courtship is associated with the female spawning role. Two hypotheses have been proposed to account for this pattern. The egg trading hypothesis states that the pattern results from competition for fertilizations and assumes that reproductive success (RS) as a male is limited by access to eggs and that female RS is not limited by access to sperm. The gamete trading hypothesis states that the pattern results from eggs being at substantial risk of not being fertilized — i.e. female RS is limited by access to sperm. An analysis was performed of data from the black hamlet and three other serranines to determine whether significant sperm limitation occurs. The evidence fails to support the hypothesis that access to sperm limits female RS. Unspawned eggs were not found in fish collected outside the spawning period, but fish without eggs always had milt (sperm). The percentage of eggs fertilized did not decrease over the course of a spawning bout. There was also a slight positive correlation between the number of eggs released in a spawning and the percentage that were fertilized, and serranines that divide the clutch into parcels do not tend to have higher fecundities than those that do not. The gamete trading hypothesis can therefore be rejected for H. nigricans.     

Sperm velocity and its relation to social status in Arctic charr (Salvelinus alpinus)

Sperm velocity has been shown to be a major determinant of fertilization success of external fertilizers. Yet, sperm velocity varies both within and between ejaculates and only a small number of fast sperm cells within an ejaculate are likely to have the potential of fertilizing the eggs. Having such fast cells should be of special importance during sperm competition, particularly for subordinate males that may release their sperm later or further away from eggs, than dominants. We examined ejaculates of dominant and subordinate male Arctic charr (Salvelinus alpinus), a species with sperm competition. Yet, rather than examining just average sperm velocity values, the aim was to examine whether the fastest fraction of sperm cell from dominant and subordinate males differed in velocity. While there was no difference in the average sperm velocity between dominant and subordinate males, analysis of the fastest swimming sperm cells show that subordinate males have significantly higher initial sperm velocity than dominant males within the 10, 5 and 1% fastest sperm cells. That is, the difference in sperm velocity between dominant and subordinate charr is most predominant among the fastest sperm cells. In sum, this study emphasizes the importance of studying the fastest sperm cells in the ejaculates, as status-dependent differences in sperm velocity may not be detected using average values.     

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.     

Reproductive biology of the rosylip sculpin, an intertidal spawner

Rosylip sculpin Ascelichthys rhodorus spawned in the intertidal during the winter in the north‐eastern Pacific. Large numbers of males typically congregated at spawning sites, where females deposited clutches. The mating system of this species was external fertilization and group spawning at specific oviposition sites under boulders in the intertidal, and no alternative male mating strategies. Males were abundant at sites while oviposition was occurring, and most abandoned the sites as spawning tapered off seasonally despite the presence of developing clutches. Experimental removal of males from sites suggested that males provided some short‐term benefits to clutches, with catastrophic loss of clutches significantly lower when males were present. The large number of males at an oviposition site and histological evidence indicating high sperm production and storage of sperm prior to release suggest a high level of sperm competition in this species. This spawning pattern appears to differ in substantial ways from any other reported fish mating system.