Reproductive biology of female big‐bellied seahorses

In this study, ovarian morphology, reproductive condition and sex steroid levels were investigated in the big‐bellied seahorse Hippocampus abdominalis , collected by snorkel and SCUBA diving in Wellington Harbour, New Zealand. Within the ovary, oocytes were contained between an outer muscular wall and an inner layer of luminal epithelium. Two germinal ridges ran along the entire length of the ovary. In cross‐section, oocytes were arranged in sequential order of development beginning at the germinal ridges and ending at the mature edge. Ovarian lamellae were absent. Vitellogenic and advanced cortical alveoli oocytes were elongated in shape, whereas maturing oocytes were distinctively pear‐shaped. Mature oocytes were large (2·6 – 4·4 mm in length) and aligned with the animal pole towards the muscular wall. Reproductively mature females were found throughout the year indicating a protracted reproductive season. The gonado‐somatic index was significantly different between all ovarian stages, but the hepato‐somatic index was not. Females with previtellogenic ovaries had significantly higher plasma concentrations of testosterone than females with vitellogenic or maturing ovaries. There was no significant difference in plasma concentrations of testosterone between females with vitellogenic or maturing ovaries, or in plasma concentrations of 17β‐oestradiol between females in all ovarian stages. This study contributes to the knowledge on the reproductive biology of female syngnathids.     

Reproductive behaviour of the black-striped pipefish Syngnathus abaster (Pisces; Syngnathidae)

The reproductive behaviour of Syngnathus abaster is described and compared with those of other syngnathids. The need for standardized behavioural data is discussed in light of the actual theories of evolution of mating patterns and sex-role reversal within this family.     

The lek mating system of the worm pipefish (Nerophis lumbriciformis): a molecular maternity analysis and test of the phenotype‐linked fertility hypothesis

The origin and maintenance of mating preferences continues to be an important and controversial topic in sexual selection research. Leks and lek‐like mating systems, where individuals gather in particular spots for the sole purpose of mate choice, are particularly puzzling, because the strong directional selection imposed by mate choice should erode genetic variation among competing individuals and negate any benefit for the choosing sex. Here, we take advantage of the lek‐like mating system of the worm pipefish (Nerophis lumbriciformis) to test the phenotype‐linked fertility hypothesis for the maintenance of mating preferences. We use microsatellite markers to perform a parentage analysis, along with a mark–recapture study, to confirm that the worm pipefish has an unusual mating system that strongly resembles a female lek, where females display and males visit the lek to choose mates. Our results show that the most highly ornamented females occupy positions near the centre of the breeding area, and males mating with these females receive fuller broods with larger eggs compared to males mating with less‐ornamented females. We also conduct a laboratory experiment to show that female ornaments are condition‐dependent and honestly signal reproductive potential. Overall, these results are consistent with the predictions of a sex‐independent version of the phenotype‐linked fertility hypothesis, as male preference for female ornaments correlates with fertility benefits.     

Behavioural temperature preference in a brooding male pipefish Syngnathus typhle

In the broad‐nosed pipefish Syngnathus typhle, brooding males positioned themselves significantly more often towards the warmer part (18° C) of an aquarium, whereas females were indifferent in this respect. This behavioural temperature preference may increase male brooding rate and indirectly influence patterns of mating competition.     

Reproductive migrations of the sex role reversed pipefish Nerophis lumbriciformis(Pisces; Syngnathidae)

Using an individual identification technique, a population of worm pipefish Nerophis lumbriciformis was followed during 19 months, in order to determine the exact use of the intertidal and, considering the specific movement patterns of males and females, the mating system exhibited by this population. Field observations showed that the number of adults increased during the breeding season, with males arriving 1 month earlier than females. Furthermore, males and females presented distinct permanence periods, showing that the intertidal is used as a mating arena. It was also observed that both male and female worm pipefish mated repeatedly over the span of a reproductive season, but females exhibited shorter remating intervals. Also, females stayed for longer periods on the mating grounds, the intertidal zone, whereas males typically left for the subtidal after mating, usually returning within 2 months. These inter‐sexual differences in the occupation of the intertidal suggest that females breed with different males but also that males accept eggs from various females since, on their return, a new group of mating partners was now available. Thus, N. lumbriciformis might be considered polygynandric. It is a clearly dimorphic species in spite of the observed polygynandry, suggesting that differences in remating intervals may be influential in determining the strength of sexual selection along with what may be expected from the polygynandrous mating system alone.     

Reproductive costs in terrestrial male vertebrates: insights from bird studies

Reproduction requires resources that cannot be allocated to other functions resulting in direct reproductive costs (i.e. trade-offs between current reproduction and subsequent survival/reproduction). In wild vertebrates, direct reproductive costs have been widely described in females, but their occurrence in males remains to be explored. To fill this gap, we gathered 53 studies on 48 species testing direct reproductive costs in male vertebrates. We found a trade-off between current reproduction and subsequent performances in 29% of the species and in every clade. As 73% of the studied species are birds, we focused on that clade to investigate whether such trade-offs are associated with (i) levels of paternal care, (ii) polygyny or (iii) pace of life. More precisely for this third question, it is expected that fast species (i.e. short lifespan, early maturity, high fecundity) pay a cost in terms of survival, whereas slow species (with opposite characteristics) do so in terms of fecundity. Our findings tend to support this hypothesis. Finally, we pointed out the potential confounding effects that should be accounted for when investigating reproductive costs in males and strongly encourage the investigation of such costs in more clades to understand to what extent our results are relevant for other vertebrates.     

Reproductive ecology of five pipefish species in one eelgrass meadow

Synopsis Synopsis Pipefishes have rarely been watched in the wild and have never before been followed in their common seagrass habitats. This study explores the reproductive ecology of five species of pipefishes living in a Swedish eelgrass meadow during parts of four breeding seasons, tagging four of the species. Pipefish are remarkable for their specialised paternal care: only males aerate, osmoregulate and nourish the developing embryos. Two of the species (Entelurus aequoreus andNerophis ophidion) have simple ventral gluing of eggs on the trunk while three species (Syngnathus acus, S. rostellatus andS. typhle) have fully enclosed brood pouches on their tails. Males of the former species receive eggs from one female while males of the genusSyngnathus receive partial clutches from several females. Sex ratios of adults on the site differed from equal to male-biased to female-biased, according to species.S. typhle were most numerous and were resighted most often. They were present throughout the breeding season whereas there were temporal shifts in the presence of the other species on the meadow and in some sex ratios. Most species occurred in the deeper, denser part of the meadow but there was some habitat separation by species and sex. All species tended to stay low in the eelgrass, primarily coming up above the eelgrass to display and mate. No species showed site fidelity either to a home range or to the meadow, withE. aequoreus adults spending least time on the meadow. Sexual size dimorphism differed: males were larger inS. rostellatus, the same size inS acus and smaller in the other species. Although the species overlap in habitat requirements and breeding season, the only observed interspecific interactions were abortive courtships betweenSyngnathus species.     

Reproductive strategy of the semelparous clam Gaimardia bahamondei (Bivalvia,Gaimardiidae)

Abstract. Semelparity is one of the most drastic reproductive strategies found among marine invertebrates. It is frequently found in species whose members have small adult sizes and brood embryos internally. In this study, we describe the reproductive strategy of the bivalve Gaimardia bahamondei to explore the possible causes of the association between semelparity and internal brooding. Males of this species exhibit continuous gonadal activity throughout the breeding season. Apparently continuous spawning of sperm is associated with an abundance of captured sperm in the adfrontal region of the gill filaments of both males and females. Females are capable of brooding three cohorts of embryos simultaneously while also producing three new cohorts of oocytes. This suggests that females are able to generate at least six cohorts of embryos during the breeding season. Embryos are brooded in the suprabranchial chamber and are individually surrounded by a membrane with a projecting peduncle; embryos are anchored by this peduncle to the adfrontal region of the gill filaments. Members of the youngest cohort differ in size, color, and shell ornamentation from members of the two older cohorts. There is no difference between members of the two older cohorts in size, but there is with respect to coloring and shell ornamentation. The importance of the embryonic cohorts in terms of their percentage of the total number of embryos varied among brooding females, suggesting among‐female variation in the timing of release of the oldest cohort of embryos. Members of this cohort break loose from the gills, lose their surrounding membrane, and fall into the ventral region of the suprabranchial chamber, from which they are evacuated to the exterior. Continuous sperm production in males and the production of at least six cohorts of embryos in females suggest that the costs of reproduction are high, which may partly explain the semelparity identified in this species.     

Sexual selection on female ornaments in the sex‐role‐reversed Gulf pipefish (Syngnathus scovelli)

Understanding how selection acts on traits individually and in combination is an important step in deciphering the mechanisms driving evolutionary change, but for most species, and especially those in which sexual selection acts more strongly on females than on males, we have no estimates of selection coefficients pertaining to the multivariate sexually selected phenotype. Here, we use a laboratory‐based mesocosm experiment to quantify pre‐ and post‐mating selection on female secondary sexual traits in the Gulf pipefish (Syngnathus scovelli), a sexually dimorphic, sex‐role‐reversed species in which ornamented females compete for access to choosy males. We calculate selection differentials and gradients on female traits, including ornament area, ornament number and body size for three episodes of selection related to female reproductive success (number of mates, number of eggs transferred and number of surviving embryos). Selection is strong on both ornament area and ornament size, and the majority of selection occurs during the premating episode of selection. Interestingly, selection on female body size, which has been detected in previous studies of Gulf pipefish, appears to be indirect, as evidenced by a multivariate analysis of selection gradients. Our results show that sexual selection favours either many bands or larger bands in female Gulf pipefish.     

Unusual modes of oogenesis and brooding in bivalves: the case of Gaimardia trapesina (Mollusca: Gaimardiidae)

Abstract. I describe an unusual case of follicular oogenesis in a bivalve, Gaimardia trapesina , a common marine bivalve from the Magellan Region and adjacent Sub-Antarctic waters, whose members brood their developing larvae. The gonad in G. trapesina is an acinus organ that infiltrates the perivisceral connective tissue; the walls of the acini are formed by tall, slender cells with distal nuclei, supported by a thin conjunctive tissue layer. At the onset of vitellogenesis, each developing oocyte becomes surrounded by a one-cell-thick layer of follicle cells, which may originate from the wall of the acinus. The cells form a follicle that completely encompasses single oocytes, except at the basal zone, where oocytes are in contact with the acinus wall. The follicle persists beyond the end of vitellogenesis and spawning. After gamete release, the persistent follicle participates in the attachment of ova and developing embryos to the interfilamental junctions of the inner and outer demibranchs of the gill, where embryos are incubated until hatching as late-stage pediveliger larvae. Ripe eggs are large (∼250 μm diameter), suggesting that development is entirely lecithotrophic. The follicle cells that mediate connections between developing embryos and the maternal individual probably have a mechanical role only, providing support and possibly facilitating the accommodation of a large number of embryos to maximize the branchial space available for brooding.     

Differences in fat accumulation between immature male and female Atlantic salmon Salmo salar after dietary administration of tetradecylthioacetic acid

This study provoked sex‐specific differences in fat metabolism in Atlantic salmon Salmo salar, by dietary administration of tetradecylthioacetic acid (TTA) during their first spring and winter in the sea. The effects of TTA were evaluated in June of the first spring and May of the second spring in the sea, by analysing white muscle‐fat content. Muscle fat in males and females differed significantly as a result of TTA in their diet and diet interacted with the sex of the fish. The fat content during the first spring after dietary TTA was lowered by a greater amount in females than in males, 3·1–4·3%, respectively (P < 0·05). In contrast, during the second spring, fat content was lowered by a greater amount in males than in females, 15·8–16·7%, respectively (P < 0·01). Condition factor followed a similar pattern to the muscle fat. The results indicate that the difference in male and female fat accumulation dynamics is related to sex‐specific reproduction biology of S. salar. In addition, the findings show that it is important to consider the sex of the fish and the season of the year when studying fat dynamics and reproductive biology of S. salar.     

The genetic mating system and tests for cuckoldry in a pipefish species in which males fertilize eggs and brood offspring externally

Highly variable microsatellite loci were used to study the mating system of Nerophis ophidion, a species of pipefish in which pregnant males carry embryos on the outside of their body rather than in an enclosed brood pouch. Despite this mode of external fertilization and brooding, otherwise rare in the family Syngnathidae, the genotypes of all embryos proved to be consistent with paternity by the tending male, thus indicating that cuckoldry by sneaker males is rare or nonexistent in this species. N. ophidion is a phylogenetic outlier within the Syngnathidae and its reproductive morphology is thought to be close to the presumed ancestral condition for pipefishes and seahorses. Thus, our genetic results suggest that the evolutionary elaboration of the enclosed brood pouch elsewhere in the family was probably not in response to selection pressures on pregnant males to avoid fertilization thievery. With regard to maternity assignments, our genotypic data are consistent with behavioural observations indicating that females sometimes mate with more than one male during a breeding episode, and that each male carries eggs from a single female. Thus, the polyandrous genetic mating system in this species parallels the social mating system, and both are consistent with a more intense sexual selection operating on females, and the elaboration of secondary sexual characters in that gender.     

Behavioral responses of a sex-role reversed pipefish to a gradient of perceived predation risk

Conspicuous behaviors such as courtship and mating often makeanimals susceptible to predation. When perceiving themselvesat an elevated level of risk, animals frequently reduce conspicuousbehaviors in tradeoff for a decrease in probability of beingpreyed upon. In the present study, we used two experiments toexamine the effect of perceived predation risk from cod (Gadusmorhud) on nonreproductive and reproductive behaviors in thesex-role reversed pipefish (Syngnathus typhle). In the firstexperiment, no differences due to predation risk were detectedin the nonreproductive behaviors of either males or females.In the second experiment, predation risk had significant effectson reproductive behaviors. Pipefish were allowed to court andcopulate at four different predation levels. We created predationlevels differing in perceived predation risk by controllingthe number of sensory modes through which pipefish could detectthe presence of a cod. As predation risk increased, pipefishcopulated and courted less frequently, swam alone (displayedand searched for conspecifics) less often, and waited longerbefore commencing courtship. These changes in behavior minimizedthe amount of time spent above the eelgrass and presumably reducedconspicuousness to visual predators. Pipefish also copulatedafter a smaller amount of courtship as predation risk increased,indicating that they may trade information concerning mate qualityfor a reduction in predation risk. No differences were foundin any response variable between males and females. The roleof operational sex ratios and intersexual competition in determiningwhich sex assumes greater costs in mate acquisition is questioned.     

Reproductive and physiological costs of repeated immune challenges in female Wellington tree weta (Orthoptera: Anostostomatidae)

Fitness‐related traits, such as immunity and reproduction, are typically condition dependent, and are predicted to trade off against each other because they share a pool of energy and resources. It is generally assumed that the resources and energy required for immune processes and reproduction is contained in the body fat; however, few studies quantify the effect of an immune insult on fat load. I tested the hypothesis that if mounting an immune response is physiologically costly in terms of consuming limited resources from body fat, and reproduction also relies on these resources, then an immune challenge should cause a reduction in fat load and an associated decline in reproduction. I tested this hypothesis by assaying the fat content of female Wellington tree weta (Hemideina crassidens) after repeated challenges with lipopolysaccharide (LPS), and counting the number of oviposited eggs in addition to assaying the egg protein content, a possible measure of egg quality. In line with my prediction, immune‐challenged females had significantly smaller fat loads and laid significantly fewer eggs than saline‐injected controls. Moreover, the protein content of the eggs laid by immune‐challenged females was significantly lower than that of controls. My experimental results show that an immune challenge with a non‐pathogenic stimulant increases fat consumption, which in turn limits the resources available for reproduction. These findings support the hypothesis that reproduction and immunity are condition dependent, and are traded off against each other. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 38–46.     

Planulation,larval biology,and early growth of the deep‐sea soft corals Gersemia fruticosa and Duva florida (Octocorallia: Alcyonacea)

Abstract. Although the reproductive biology and early life‐history stages of deep‐sea corals are poorly understood, such data are crucial for their conservation and management. Here, we describe the timing of larval release, planula behavior, metamorphosis, settlement, and early juvenile growth of two species of deep‐sea soft corals from the northwest Atlantic. Live colonies of Gersemia fruticosa maintained under flow‐through laboratory conditions released 79 planulae (1.5–2.5 mm long) between April and early June 2007. Peak planulation in G. fruticosa coincided with peaks in the chlorophyll concentration and deposition rates of planktic matter. Metamorphosis and settlement occurred 3–70 d post‐release. The eight primary mesenteries typically appeared within 24 h, and primary polyps grew to a height of ～6–10 mm and a stalk diameter of ～1 mm within 2–3 months. Planulae of Duva florida (1.5–2.5 mm long) were extracted surgically from several colonies and were successfully reared in culture. Primary polyps reached a height of ～3–4 mm within 2–3 months. No budding of primary polyps was observed in either species over 11–13 months of monitoring, suggesting a very slow growth rate.     

Reproductive allocation and the long-term costs of reproduction in Siparuna grandiflora, a dioecious neo-tropical shrub

1 Using a combination of observational and experimental approaches, both allocation of resources to reproduction (often called the direct cost of reproduction) and the subsequent long-term costs (the indirect, delayed or demographic cost) associated with reproductive allocation to male and female function in Siparuna grandiflora (Siparunaceae), a tropical dioecious shrub, were examined.
2 The objectives were to determine whether females allocate more biomass or nitrogen per reproductive episode than males, and whether there is a long-term cost of reproduction in terms of subsequent growth or reproduction for either sex. If there is no long-term cost of reproduction, then reproduction may be viewed as free in an evolutionary sense.
3 As is generally the case in dioecious species, females allocated more biomass and nitrogen to reproduction than males. Females also showed delayed costs of reproduction in terms of decreased growth and subsequent reproduction, whereas males did not.
4 The lack of measurable delayed costs in males suggests that with the evolution of dioecy, selection has reduced delayed costs of reproduction in S. grandiflora males. In contrast, females that were prevented from reproducing were able to re-allocate resources to growth, and produced more stem length on average than males. This re-allocation response may have evolved to reduce delayed costs of reproduction in females over time frames longer than that considered in the present study.     

Reproductive biology of the southern thorny skate Amblyraja doellojuradoi (Chondrichthyes,Rajidae)

The total lengths (L_T) of 193 males (209–556 mm) and 130 females (275–515 mm) of Amblyraja doellojuradoi, a commercial by‐catch species on the Argentinean continental shelf, which are increasingly retained, were analysed. No sexual dimorphism was observed in the L_T at which 50% of individuals were sexually mature; males matured at 448 mm and females at 411 mm, c. 80 and 82% of maximum L_T. The hepato‐somatic index was similar among sexes, but significantly different between maturity stages, being lower in mature than immature specimens. Males had no seasonal difference in the hepato‐somatic index and females had the lowest index in autumn. The gonado‐somatic index was lower in males than in females and significantly higher in mature than immature specimens of both sexes. Males had the highest index in autumn and females had no seasonal difference. Collectively, these results would indicate that A. doellojuradoi breeds in autumn.