Costs of parental care on hunting behaviour of Helobdella papillornata (Euhirudinea: Glossiphoniidae)

Helobdella papillornata, an Australian freshwater leech, feeds primarily on snails and has a high level of parental care involving brooding eggs and young, with direct feeding of young. Parental costs and offspring benefits from these behaviours are poorly understood. A potential cost of parental care may be a change in the time taken to hunt prey. To test this hypothesis, the hunting behaviour of adults without progeny, parents with eggs, and parents with young were compared. We found that parents brooding eggs had a significantly (P = 0.029) longer lag time to begin hunting than parents brooding young, and spent significantly (P = 0.018) less time actively hunting than non-brooding adults. These costs, which may represent lost potential for the parent’s future reproductive success, should be outweighed by the fitness benefits of improved growth and survival of offspring, if parental care is favoured by selection. The hunting costs of care in Helobdella and other benthic, dorsoventrally flattened leeches in the family Glossiphoniidae may be smaller than the costs of brood tending that would be imposed on other freshwater leeches, and this difference may help explain the restriction of care to a single clade of the Euhirudinea.     

Reproductive Behaviour and Parental Care of Helobdella striata (Hirudinea,Glossiphoniidae): a Leech that Feeds its Young

The leech Helobdella striata Kutschera (1985) is a protandrous hermaphrodite. It copulates by hypodermic injection: a spermatophore is attached to the skin of the partner and sperm injected through it. During their male phase, the leeches copulate repeatedly and with different partners. In the female phase, 3 to 7 cocoons, each containing 2 to 20 eggs, are produced from the female gonopore and attached to the ventral side of the parent. The larvae which hatch from these eggs cling to the ventral side of the parent. After they have used up their yolk supply and have developed into juvenile leeches they remain attached to the parent for a further three weeks. Helobdella striata capture Tubifex worms and give them to the young they carry. This access to food allows the juveniles to grow from a size of 1 mm to 6 mm length while being carried and protected by the parent. H. striata reared in isolation produce young; at present it is not known whether they reproduce by parthenogenesis or by self-fertilization. The probable phylogenetic development of parental care patterns in the Hirudinea is reviewed.     

Does maternal care evolve through egg recognition or directed territoriality?

The mechanism that facilitates the evolution of maternal care is ambiguous in egg‐laying terrestrial vertebrates: does the ability of mothers to recognize their own eggs lead them under some circumstances to begin providing care or can maternal care evolve from simply being in close proximity to the eggs (e.g. through territorial behaviour)? This question is difficult to answer because in most species, parental care is either absent altogether or present; in only a few species we have the opportunity to observe intraspecific variation in the expression of parental care. We studied a population of long‐tailed skinks (Eutropis longicaudata) in which females have recently evolved maternal care from a noncaring state. Females on Orchid Island, Taiwan, remain with their eggs during incubation and when doing so, actively deter egg predation by egg‐eating snakes (Oligodon formosanus); in all other populations, females lack post‐ovipositional maternal care. Nest‐guarding females on Orchid Island (i) showed antipredator behaviours only in the original nest site in which they laid eggs, even after we removed all of the eggs or substituted them with those of a conspecific; (ii) protect any eggs present inside the original nest site (even when the eggs belong to a conspecific); and (iii) develop this behaviour while gravid (i.e. prior to laying eggs). This supports the hypothesis that long‐tailed skinks cannot recognize their own eggs, suggesting that maternal care is a directed form of territoriality only expressed towards egg‐eating snakes and only during reproduction. Nest guarding is among the most primitive forms of parental care, and the recent evolution of this behaviour in a single population provides insight into one of the mechanisms by which parental care can originate in terrestrial vertebrates.     

Predatory risk increased due to egg‐brooding in Armadillidium vulgare (Isopoda: Oniscidea)

Cost of reproduction is associated with a reduction in subsequent survival or future breeding success. A decrease in survival rate of parents during or after reproduction reduces the probability of their future reproduction. However, few studies have demonstrated such survival costs to parents. Females of Armadillidium vulgare hold their eggs in a marsupium and brood these until the young hatch. Caring for eggs in a marsupium seems to place a large burden on brooding females, and it restricts their predator avoidance behaviour. As such, costs of care may increase the mortality rates of brooding females. To reveal the costs of parental care, we examined the effects of egg brooding on behaviour and predation risk. Egg‐brooding females decreased speed of locomotion and rolling duration, and were killed by predators at a higher rate. Our results indicate that egg brooding in A. vulgare has costs in the form of predation risk.     

Sexual behavior,insemination and development of the freshwater leech Helobdella stagnalis (Annelida,Hirudinea, Glossiphoniidae)

The reproductive biology of the Glossiphoniidae leech Helobdella stagnalis, under laboratory conditions, the structure of its eggs and its developmental stages were studied. Sperm transfer and insemination are made by hypodermic injection: one or numerous spermatophores were attached to the skin of the partner during copulation and sperm is injected through it. The leeches can copulate repeatedly with several partners. Each leech produces 4–8 cocoons containing 20–60 eggs whose are attached to the ventral side of the parent and carried around. At 22 °C, the developmental duration is 24 days from the oviposition until the juveniles leave the parent leech. Three (3) major stages have been distinguished: Eggs cleavage, germinal band generation, and juveniles hatching. The sexual behavior of Hellobdella stagnalis was described with a special attention given to parental care.     

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.     

Rapid and convergent evolution of parental care in hydrobiid gastropods from New Zealand

Although parental care occurs in most phyla encompassing a wide array of forms, little is known about its evolution in invertebrates. Two types of egg capsules have been known among ovoviviparous New Zealand hydrobiid gastropods, elastic capsules and simple membranes. Based on a phylogenetic analysis using two mtDNA sequence fragments, I asked whether the second state was derived from the first or whether brooding had multiple origins. The evolution of ovoviviparity was also investigated in the context of habitat transition between brackish and freshwater. Maximum parsimony and Markov chain models of character state transformations in a maximum likelihood framework suggested that hydrobiids have invaded freshwater three times independently. Two of these invasions were followed by the evolution of ovoviviparity, probably in adaptation to changing water levels during periods of irregular precipitation. The syntopy of two congeneric species, one oviparous and the other one brooding, indicated that the transition between reproductive modes must have occurred rapidly.     

The dynamics of male brooding,mating patterns,and sex roles in pipefishes and seahorses (family Syngnathidae)

Modern theory predicts that relative parental investment of the sexes in their young is a key factor responsible for sexual selection. Seahorses and pipefishes (family Syngnathidae) are extraordinary among fishes in their remarkable adaptations for paternal care and frequent occurrences of sex-role reversals (i.e., female-female competition for mates), offering exceptional opportunities to test predictions of sexual selection theory. During mating, the female transfers eggs into or onto specialized egg-brooding structures that are located on either the male's abdomen or its tail, where they are osmoregulated, aerated, and nourished by specially adapted structures. All syngnathid males exhibit this form of parental care but the brooding structures vary, ranging from the simple ventral gluing areas of some pipefishes to the completely enclosed pouches found in seahorses. We present a molecular phylogeny that indicates that the diversification of pouch types is positively correlated with the major evolutionary radiation of the group, suggesting that this extreme development and diversification of paternal care may have been an important evolutionary innovation of the Syngnathidae. Based on recent studies that show that the complexity of brooding structures reflects the degree of paternal investment in several syngnathid species, we predicted sex-role reversals to be more common among species with more complex brooding structures. In contrast to this prediction, however, both parsimony- and likelihood-based reconstructions of the evolution of sex-role reversal in pipefishes and seahorses suggest multiple shifts in sex roles in the group, independent from the degree of brood pouch development. At the same time, our data demonstrate that sex-role reversal is positively associated with polygamous mating patterns, whereas most nonreversed species mate monogamously, suggesting that selection for polygamy or monogamy in pipefishes and seahorses may strongly influence sex roles in the wild.     

Male parental care and its adaptive significance in a neotropical frog

In the Puerto Rican frog Eleutherodactylus coqui, parental care is performed exclusively by males, and consists of attending the eggs and hatchlings at a terrestrial oviposition site. The two major behavioural components of parental care are egg brooding and nest defence against conspecific egg cannibals. Defence behaviour includes aggressive calling, biting, sustained biting, wrestling, and blocking directed against nest intruders. Parental care lasts from oviposition to hatching (17–26 days) and often for several days after hatching. During pre-hatching development, males are present in their nests 97.4% of the time during the day and 75.8% of the time at night. A large portion of this time is spent brooding eggs. In a field experiment, males were removed from their nests and the fate of clutches was monitored. Compared to control clutches (males not removed), experimental clutches had significantly lower hatching success and suffered significantly greater mortality from desiccation and cannibalism. Hence, parental care yields significant benefits to male fitness via increased offspring survival.     

The life-cycle,ecology and host specificity of the freshwater leech Alboglossiphonia polypompholyx (Glossiphoniidae) in Egypt

Alboglossiphonia polypompholyx spends most of its life cycle endoparasitic in the mantle cavity of the snail Bulinus truncatus — possibly its only host. Adult A. polypompholyx leaves the snail about one month before the commencement of egg-laying. Hatching occurred after about 15 d and after brooding on the venter of the parent for 7–10 d, the young briefly become free-living before entering the mantle cavity of B. truncatus. Within the mantle cavity, A. polypompholyx feeds and grows for 16–20 weeks before leaving the snail as adults. In the field and in laboratory experiments, adult leeches left the snails in August/September and January with cocoons produced in October/November and February/March, respectively. Free-living adult leeches do not feed and die 1–2 months after the cessation of brooding.     

Evolution of parental care and ovulation behavior in oysters

Approximately half of all living oysters brood offspring in the inhalant chamber of their mantle cavities; the remainder are broadcast spawners which do not engage in parental care of young. Ostreid ovulation involves a complex behavioral sequence that results in the countercurrent passage of newly spawned eggs through the gills (ctenidia) and into the inhalant chamber. We constructed molecular and combined-evidence phylogenetic trees to test hypotheses concerning the directionality of parental care evolution, and the evolutionary significance of the trans-ctenidial ovulation pathway, in the Ostreidae. Representatives of all three ostreid subfamilies, together with gryphaeid and nonostreoidean pterioid outgroups, were sequenced for a 941-nucleotide fragment of the 28S ribosomal gene. Our phylogenetic analyses indicate that (1) the Ostreidae are robustly monophyletic, (2) broadcast spawning and larval planktotrophy are ancestral ostreid traits, (3) trans-ctenidial ovulation predates the evolution of parental care in ostreid lineages, and (4) brooding originated once in the common ancestor of the Ostreinae/Lophinae, involved a modification of the final behavioral step in the ancestral ovulation pathway, and has been retained in all descendent lineages. Our data permit an independent test of fossil-based ostreid phylogenetic hypotheses and provide novel insights into oyster evolution and systematics.     

The lack of influence of exogenous testosterone on male parental behavior in a neotropical frog (Eleutherodactylus): a field experiment

Males of the Puerto Rican frog Eleutherodactylus coqui exhibit prolonged parental care (nest attendance and defense) of direct-developing eggs in nonaquatic nest sites. Earlier work showed that plasma androgen levels are significantly lower in males caring for eggs than in noncaring, calling males. In this study, we investigated the effects of elevated plasma androgens on parental care behavior by implanting either testosterone (T) or placebo (P) pellets in parental males brooding eggs in the field. Plasma androgen levels, assessed 4 days after pellet implantation, were six times higher in T males than in P males. Despite this increase, T males exhibited no changes in nest fidelity or brooding behavior. The results indicate that lower androgen levels, at least those corresponding to a decline in T during parental care, are not necessary to maintain parental behavior in this tropical frog.     

Terrestrial reproduction and parental care drive rapid evolution in the trade-off between offspring size and number across amphibians

The trade-off between offspring size and number is central to life history strategies. Both the evolutionary gain of parental care or more favorable habitats for offspring development are predicted to result in fewer, larger offspring. However, despite much research, it remains unclear whether and how different forms of care and habitats drive the evolution of the trade-off. Using data for over 800 amphibian species, we demonstrate that, after controlling for allometry, amphibians with direct development and those that lay eggs in terrestrial environments have larger eggs and smaller clutches, while different care behaviors and adaptations vary in their effects on the trade-off. Specifically, among the 11 care forms we considered at the egg, tadpole and juvenile stage, egg brooding, male egg attendance, and female egg attendance increase egg size; female tadpole attendance and tadpole feeding decrease egg size, while egg brooding, tadpole feeding, male tadpole attendance, and male tadpole transport decrease clutch size. Unlike egg size that shows exceptionally high rates of phenotypic change in just 19 branches of the amphibian phylogeny, clutch size has evolved at exceptionally high rates in 135 branches, indicating episodes of strong selection; egg and tadpole environment, direct development, egg brooding, tadpole feeding, male tadpole attendance, and tadpole transport explain 80% of these events. By explicitly considering diversity in parental care and offspring habitat by stage of offspring development, this study demonstrates that more favorable conditions for offspring development promote the evolution of larger offspring in smaller broods and reveals that the diversity of parental care forms influences the trade-off in more nuanced ways than previously appreciated.

What selective pressures alter the tradeoff between offspring size and number? A phylogenetic comparative approach shows that amphibians with direct development and those that lay eggs in terrestrial environments have larger eggs and smaller clutches, while different care behaviours and adaptations vary in their effects on the tradeoff.     

Male pregnancy in seahorses and pipefishes (family Syngnathidae): rapid diversification of paternal brood pouch morphology inferred from a molecular phylogeny

In contrast to the majority of vertebrate species, primary male parental care is common in fishes and encompasses a remarkable diversity of adaptations. Seahorses and pipefishes (Family Syngnathidae) exhibit some of the most specialized forms of paternal care in animals and so are ideally suited to the study of the evolution of male parental care. During mating, female syngnathids transfer eggs to specialized morphological structures that are located on either the abdomen or tail of the male. The male provides all postfertilization parental care and has morphological and physiological adaptations to osmoregulate, aerate, and even nourish the developing embryos. While all syngnathid species are adapted for paternal care, the brooding structure with which this is accomplished varies between species, from simple ventral gluing areas to much more complex structures such as the completely enclosed pouches of the seahorses. Our combined cytochrome b-, 12S rDNA-, and 16S rDNA-based molecular phylogeny of syngnathid fishes demonstrates that rapid diversification of male brooding structures has been associated with the major evolutionary radiation of the group, suggesting that development and diversification of structures involved in paternal care may have been key evolutionary innovations of the Syngnathidae. Molecular analyses also highlight geographical centers of biodiversity and suggest interoceanic migration of Syngnathus pipefishes from their center of origin in the Pacific.     

Nest, but Not Egg, Fidelity in a Territorial Salamander

Egg recognition and subsequent egg brooding are costly forms of parental investment in many species of vertebrates. Life history factors, such as coloniality or risk of brood parasitism, may constrain egg recognition in vertebrates. Female red-backed salamanders ( Plethodon cinereus ) from my study site are territorial and do not share nest sites with other females. They are terrestrial and neither they nor their eggs are likely to be displaced by environmental factors such as flooding. I experimentally tested, in the laboratory, the hypothesis that female red-backed salamanders can discriminate between their own eggs and the eggs of unfamiliar females. Each female was allowed to move about a test chamber containing two clutches of eggs, one clutch with which it was found in the forest and one that had been found with a distant female. Most females remained with one clutch of eggs, which they brooded during the entire observation period. However, they did not significantly prefer to brood their own eggs over the eggs of another female. In a corollary field experiment, I tested whether brooding females that were displaced 1 m from their nest sites would return to their territories and commence brooding behaviour within 3 d. All 10 displaced females returned to their own nest within this time period and were found brooding their eggs. Because female red-backed salamanders at my study site do not tend to share nest sites with other females and because their eggs remain in stationary nests, selection may not have favoured egg recognition. However, the results suggest that female salamanders indirectly recognize their own eggs by actively recognizing their territorial nest sites.     

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.     

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.     

Behavioural insensitivity to supplementary testosterone during the parental phase in the chestnut-collared longspur,Calcarius ornatus

In seasonally breeding male birds that show paternal care, plasma testosterone (T) peaks in the early spring coincident with territory establishment and pair bonding. Once nests are initiated, T declines precipitously and remains low as nestlings hatch and males become parental. A growing body of evidence suggests there is a trade-off between a male's level of T and his expression of paternal care: high T enhances sexual behaviour but reduces paternal care. Male chestnut-collared longspurs show high levels of paternal care. They feed and brood young, act as nest sentries and aggressively defend the nest against predators. We experimentally altered males' plasma levels of T such that the early spring T peak was extended through the parental phase. T enhanced song behaviour typical of the sexual phase and decreased nest sentry behaviour during incubation, but did not reduce brooding or feeding of nestlings. Thus, males responded behaviourally to T during incubation, but, unlike most other temperate-breeding birds studied, did not respond to T after eggs hatched. Based on these data and similar results in an Arctic passerine, we suggest that the pattern of males' reduced responsiveness to T during the nestling phase may reflect the relative importance of male care to nest success in this species, or a phylogenetic constraint common to the genusCalcarius . Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

A comparative survey of the Erpobdella octoculata (L.) populations in the Afon Crafnant,N. Wales,above and below an input of zinc from mine-waste

The life-cycle, growth, and reproductive success of a stream-dwelling Erpobdella octoculata (L.) were studied over a 19-month period at two sites, one above and one below an input of zinc pollution from mine-waste. Samples were collected monthly using quadrats. The blotted wet weight of all leeches was measured. An histological technique was employed to determine sexual maturity. Reproductive success was measured by estimating the numbers of cocoons and number of eggs per cocoon at each site. A wet ashing technique, followed by analysis using flame atomic absorption spectrometry, was used to determine the extent of bioaccumulation of zinc. Total zinc and other metals in the waters were similarly analysed.Differences were found between the populations at the two sites. The life-history of the Erpobdella above the contamination was comparable to that found for other stream-dwelling populations previously studied. Observed differences in densities of leeches between sites in the present and in previous studies by other workers may be due to recorded differences in the abundance of available food. At the polluted site, there was evidence that (a) there was a delay in cocoon deposition and hence hatching of young, (b) the adult leeches produced more misshapened and empty cocoons, (c) no relationship existed between the area of cocoons with eggs and number of eggs present, and (d) the proportion of young to adult leech was smaller at the polluted site. At the polluted site, higher levels of zinc were recorded in the tissues of Erpobdella and there was some evidence for the active intake of zinc by the leech.     

Brooding in echinoderms: How can modern experimental techniques add to our historical perspective?

Echinoderms are among the most abundant and ecologically successful groups of marine animals on earth. Their unique adaptations have enabled them to inhabit diverse environments ranging from various substrates in shallow water habitats to the benthos of the deepest seas. Although members of the Echinodermata generally share common characteristics including radial symmetry, a unique water vascular system, and decentralized cephalization, they have evolved a variety of life history strategies that enable them to reproduce successfully across a wide range of habitats. These reproductive strategies range from a complete lack of parental care (broadcasting) to internal and external brooding of the eggs, embryos, and juvenile phases. Although brooding is relatively rare in echinoderms, it is of interest as a “deviant” or “derived” form of reproduction that has been the subject of much study and debate. The aim of the present review is to examine how and why brooding occurs from a historical perspective, and then explore how modern experimental techniques are providing novel approaches to answering fundamental questions related to brooding in this very successful group of benthic marine invertebrates.