Effects of egg removal on maternal aggression, biogenic amines, and stress indicators in ovigerous lobsters (Homarus americanus)

In many disparate taxa, including crayfish, a freshwater decapod crustacean, the presence of one's offspring has been shown to be an important variable in the level of maternal aggression. Ovigerous American lobsters (Homarus americanus) show a territorial advantage against nonmaternal females, even though no posthatch care is provided. The eggs are attached to the pleopods (swimmerets) throughout embryogenesis. We evaluated the effect of stripping ovigerous H. americanus females of their eggs on maternal territoriality. In one treatment group, maternal females were stripped of all eggs. Twelve days later, including being individually isolated for an additional 48 h in a test tank, each resident was serially intruded upon by 4 non-maternal conspecific females. An identically treated control group of ovigerous female residents was left intact prior to the serial intrusions. Various biochemical parameters of the stripped and unstripped animals were measured before and after the experimental treatment (or control). The behavioral modulators measured were the biogenic amines, octopamine and serotonin, and the stress indicators were a heat-shock protein (HSP70), methyl farnesoate, and crustacean hyperglycemic hormone. The intact ovigerous residents showed a significant territorial advantage over the intruders, whereas the contest outcomes of stripped residents were reduced to chance. The presence of eggs in maternal H. americanus is therefore necessary for the maintenance of the shelter-related territorial advantage. However, no significant differences in any of the biochemical parameters were observed between or within treatment conditions. It appears that these amines are not prominently involved in the mechanism of maternal aggression, and that these changes in territorial defense are not simply due to changes in general stress as a result of stripping the females of their eggs.     

Chemical egg defence in the large milkweed bug,Oncopeltus fasciatus,derives from maternal but not paternal diet

Many herbivorous insects sequester defensive compounds from their host‐plants and incorporate them into their eggs to protect them against predation. Here, we investigate whether transmission of cardenolides from the host‐diet to the eggs is maternal, paternal, or biparental in the large milkweed bug, Oncopeltus fasciatus (Dallas) (Hemiptera: Lygaeidae). We reared individual bugs on either milkweed seeds [MW; Asclepias syriaca L. (Apocynaceae)] that contain cardenolides, or on sunflower seeds [SF; Helianthus annuus L. (Asteraceae)] that do not contain cardenolides. We mated females and males so that all four maternal/paternal diet combinations were represented: MW/MW, MW/SF, SF/MW, and SF/SF. Using larvae of the common green lacewing, Chrysoperla (Chrysopa) carnea (Stevens) (Neuroptera: Chrysopidae), we conducted two‐choice predation trials to assess whether maternal, paternal, or biparental transmission of cardenolides into the eggs of O. fasciatus increased protection against predation. Furthermore, we used high performance liquid chromatography (HPLC) to assess putative cardenolide content of eggs from the various parental diet treatment groups. The predation trials suggested that regardless of male diet, eggs were afforded better protection when females had been raised on milkweed. However, many eggs were at least partially consumed. This suggests that although chemical defence of eggs does not guarantee protection to eggs on an individual basis, they may increase the probability that some eggs in a clutch are left intact thereby potentially conferring a fitness advantage to more offspring than if eggs are left unprotected. Based on HPLC analysis we found that maternal contribution of cardenolides was significantly greater than paternal contribution of cardenolides to the eggs, supporting the results of our predation trials that a maternal diet of milkweed makes eggs more distasteful than a paternal diet of milkweed.     

Disruption of Dear Enemy Recognition Among Neighboring Males by Female Leon Springs pupfish, Cyprinodon bovinus

Males defending territories often settle into adjacent areas, sharing a common border that is maintained by a reduced level of aggression known as dear enemy recognition. While social conditions may affect the dear enemy relationship among males, what role females play, if any, is unclear. In a field study of the highly promiscuous Leon Springs pupfish, Cyprinodon bovinus, we asked whether females influenced this relationship of neighbors to their advantage. We observed 16 territorial residents, mapping the precise location of each male's behaviors within its territory. Resident males engaged in less aggression against neighbors compared with intruders, and neighbors intruded less deeply into the residents’ territories than intruders. Despite this locality restriction, neighbors were responsible for as many spawning interruptions as intruders. Females did not spawn randomly in the males’ territories, nor did they spawn near territory centers where aggression was low. Rather, females were more likely to settle and spawn in the outer half of the territories where competition among males was highest. When a neighbor entered a resident's territory to interrupt a spawn, the female was more likely to leave the resident's territory for the neighbor's than to remain. These observations suggest that the female used the intrusion by the neighbor to engage the resident and interrupt the spawn as a measure of this male's quality and that, while neighboring males benefit from the presence of dear enemy recognition, females benefit from its disruption.     

The effect of temperature and water quality on the in vitro development and survival of Asellus aquaticus (Crustacea: Isopoda) eggs

The rate of development and degree of survival of Asellus aquaticus eggs outside the marsupium of ovigerous females are affected by water quality and temperature. Eggs were maintained in polluted river water and relatively clean canal water. Developmental rates increase with increased temperature, but survival decreases. Eggs from polluted site ovigerous females survive better in clean water than in polluted water. Eggs from clean site ovigerous females maintained in polluted water have significantly lower survival rates than eggs from the polluted site at all temperatures tested. The developmental rate of clean site eggs is increased significantly in polluted water at 10–25 °C, possibly as a response to the stress imposed upon them.It is suggested that the method outlined might form the basis of a useful bioassay technique for measuring water quality.     

Female reproductive pattern of Callinectes sapidus Rathbun, 1896 (Brachyura: Portunidae) in Iskenderun Bay,Eastern Mediterranean

We studied the female reproductive pattern of Callinectes sapidus, which was introduced to the Mediterranean in the 20^th century. We assessed female size at first maturity, fecundity, and fecundity relationship to size in Iskenderun Bay, eastern Mediterranean, Turkey. Samples were collected between July 2014 and June 2015 using bottom trawling at depths ranging from 1 to 50 m. A total of 322 crabs were caught of which 308 (95.7%) were females including 116 ovigerous ones. The minimum carapace width of the mature females was 39.1 mm and the mean carapace width 123.8 mm. The carapace width of ovigerous females varied between 95.1 and 144.5 mm, with a mean of 120.3 mm. The highest number of ovigerous females was observed in July and August. Mean fecundity was 1.91 million (667,950–4,669,853) eggs per female. A weak positive linear relationship between fecundity and carapace width was noted, as well as a high correlation with total egg weight. In the eastern Mediterranean, maturity sizes of females were smaller than those in the native region of the species.     

Breeding Season Aggression of Female and Male Eastern Bluebirds (Sialia sialis) to Models of Potential Conspecific and Interspecific Egg Dumpers

Naturally occurring aggression between female eastern bluebirds (Sialia sialis) is dramatic, resulting in severe injuries and even death. Furthermore, aggression among bluebirds is usually sex specific: males attack males, females attack females. We hypothesized that the primary function of female-female aggression is to guard against the threat of intraspecific egg dumping and that, in this context, same sex aggression is related to the possibility of advantages for males of parasitism (egg dumping) of their nests. Our hypotheses to explain variation in naturally occurring aggression predict temporal variation in aggressive tendency within nest cycles and between the sexes depending on asymmetries in threats to the residents. We report the results of experimental trials in the field designed to determine temporal variation in the aggressive tendencies of resident females to models of intruder females of two species, eastern bluebirds and brown-headed cowbirds (Molothrus ater). Both species dump eggs in the nests of bluebirds. Female aggression to eastern bluebird models is greatest during early stages of nest cycles; the patterns are most consistent with protection against egg dumping and protection of nest sites from usurpation. Male residents seldom attack female eastern bluebird models, but often attack models of female brown-headed cowbirds, a result inconsistent with the hypothesis that patterns of differential parental care control aggression of female and male residents.     

Reproductive pattern of the freshwater prawn Pseudopalaemon bouvieri (Crustacea,Palaemonidae) from hypo-osmotic shallow lakes of Corrientes (Argentina)

Pseudopalaemon bouvieri undergoes complete abbreviated development. The reproductive cycle (proportion and size of the sexually mature population and juvenile recruitment), fecundity and egg size of this prawn were examined in three subtropical shallow lakes. The reproductive cycle was seasonal; gonadal maturation occurred during the winter, ovigerous females were abundant in the spring and breeding occurred at the end of spring. Females produced small numbers of eggs (9–55) of relatively large sizes (1.0–2.1 mm). The proportion of ovigerous females with respect to the total number of females, the fecundity and egg size differed among the lakes according to the trophic state of the environments. Pseudopalaemon bouvieri has a reproductive strategy similar to other Palaemonidae species that inhabit nutrient-poor inland waters.     

Information on Resource Quality Mediates Aggression between Male Madagascar Hissing Cockroaches, Gromphadorhina portentosa (Dictyoptera: Blaberidae)

Male Madagascar hissing cockroaches, Gromphadorhina portentosa Schaum (Dictyoptera: Blaberidae) have a well‐defined dominance hierarchy that has been assumed to explain the outcome of most competitive interactions. We studied whether males of this species would alter their level of aggression towards unfamiliar rivals as a function of changing resource availability and value – two factors that are key to aggression levels in non‐hierarchical species. We quantified male aggression as three variables (aggressive state – behaviours measured by their duration; aggressive act – behaviours measured by their frequency of occurrence; aggressive latency – the latency to first aggressive behaviour, either state or act) and tested for any context‐specific variation within each by manipulating both territorial status (males were either residents or intruders) and access to mates (female present or absent). Both the presence of a female and territorial status affected male aggression towards rivals as measured by duration of aggressive state. Highest levels of aggression were displayed by residents when a female was present. These results show that inter‐male aggression in G. portentosa is tuned to the immediate expected payoff from fighting, and not exclusively aimed at establishing dominance relationships (which can affect future payoffs).     

Heart rate and gill ventilation in ovigerous and non‐ovigerous edible crabs,Cancer pagurus: The effects of disturbance,substrate and starvation

This study compared the cardiac and ventilatory behaviour of disturbed and settled (48 h recovery) ovigerous Cancer pagurus with the behaviour of non‐ovigerous crabs. It also examined the effects of starvation and a sand substrate on ovigerous females. Ovigerous crabs had significantly lower heart rates than non‐ovigerous crabs. This implies that they have a reduced metabolic rate, confirmed by an earlier study which described lower rates of oxygen uptake in ovigerous crabs. Scaphognathite beat frequency was unaffected by either the presence of eggs, starvation or a sand substrate, but the amplitude of ventilatory pressure changes was higher in settled ovigerous females, implying greater force. The duration of periods of reversed ventilation was also substantially extended in ovigerous crabs, and disturbance caused a ten‐fold increase in the frequency of these reversals, resulting in ventilation being carried out in a predominantly reversed direction. It is suggested that these respiratory adaptations serve to ventilate the egg mass. Disturbance also led to a greater elevation of heart rate in ovigerous crabs, indicating that they are more prone to handling stress. Fed ovigerous crabs spent a higher percentage of time ventilating unilaterally; this response was lost following starvation. Starved ovigerous crabs had the lowest mean heart rate, highest mean ventilatory pressures and, when disturbed above a sand substrate, they showed the highest frequency of reversals of ventilation, possibly in association with their efforts to bury their abdomen bearing the egg mass.     

Reproductive success in male sunbleak, a recent invasive fish species in the U.K.

The spawning behaviour of male nest guarding sunbleak Leucaspius delineatus , a recent invasive species in southern England, was studied and quantified for the first time. In the absence of physical differences between territorial and non‐territorial males ( i.e . colour, size, etc .), the reproductive behaviour of territorial males was analysed and related to reproductive success. The results showed that females preferred high‐courting and highly aggressive males. The initial cue in female mate choice, however, was based on courtship, while aggression was the decisive behavioural trait in influencing mate choice, providing a direct signal of physical condition and 'paternal competence'. Some males picked nest sites which were subsequently preferred by other males taking over the nest of a previous male ('communal nest'), with the new territorial male adopting the eggs already present at the nest. It appears that either due to female preference for nests already containing eggs or lower rates of sired egg predation by dilution among unrelated eggs, sunbleak males have adopted the mating strategy of allopaternal care.     

Ovigerity,selective predation,and variable diel vertical migration in Euchaeta elongata (Copepoda: Calanoida)

Summary We present a statistical analysis of a previously published (Yen, 1983) but heretofore unanalyzed data set on the vertical distributions and diel vertical migration (DVM) of adult females of the marine planktonic copepod Euchaeta elongata in Dabob Bay, Washington, USA. Non-ovigerous females were strongly migratory on all four dates sampled, residing between 75–175 m during the day and at shallower depths during the night, commonly entering the upper 50 m of the water column. In contrast, ovigerous females were non-migratory or weakly migratory, largely remaining between 100–175 m both day and night, and entering the upper 50 m of the water column only rarely. Thus non-ovigerous females always migrated much more strongly, as measured by both amplitude of migration and the proportion of animals migrating, than did ovigerous females. These results led us to hypothesize that differential susceptibility to visually orienting predators was the cause of these differences in DVM behavior in female E. elongata, and we subsequently undertook an experimental study of the feeding selectivity of the copepod's natural predator, Pacific herring (Clupea harengus pallasi). Pacific herring exhibited a highly significant preference for ovigerous over nonovigerous adult female E. elongata. The demographic consequences of variable DVM in adult female E. elongata were investigated by way of life table analyses. Results indicated that under conditions of thermal stratification of the water column there is a distinct demographic disadvantage (reduced rate of realized population growth) incurred by non-migratory or weakly migratory ovigerous females due to delayed egg development at cooler subsurface temperatures. We conclude that ovigerous female E. elongata remain at depth both day and night to avoid visually orienting predators, and that such behavior must afford the copepod a demographic advantage of no less than a 26% reduction in adult mortality to offset the demographic cost of delayed egg development.     

Sex and reproductive stage differences in the growth,metabolism, feed,fecal production,excretion and energy budget of the Amazon River prawn (Macrobrachium amazonicum)

The aim of this study was to evaluate differences in various physiological measures (growth, fecal production, feed intake, nitrogenous excretion, oxygen consumption, energy substrate used, and energy budget) among males, ovigerous females and non-ovigerous females of the freshwater prawn Macrobrachium amazonicum. This species exhibits pronounced sexual dimorphism and different male morphotypes and has the potential for use in aquaculture. Males and non-ovigerous females were studied for 30?days. Ovigerous females were studied for 10?days. Prawns were fed commercial prawn food, and all males were of the Translucent Claw (TC) morphotype. The results demonstrate physiological differences both between males and females and between females of different reproductive stages. Males had higher rates of ingestion, growth and oxygen consumption and less fecal loss than females. We postulate that in the absence of other morphotypes, TC males may exhibit increased growth rates. Males and females used protein as an energy substrate. Males channeled approximately 9% of their energy budget into growth, whereas non-ovigerous and ovigerous females channeled only 1.4?±?0.4 and 0.07?±?0.07%, respectively. Whereas males and non-ovigerous females channeled 9.0?±?9.74 and 61.8?±?3.0%, respectively, of the energy ingested into metabolism, ovigerous females channeled 97.7?±?4.7% into metabolism, likely due to the frequent beating of their pleopods, which oxygenates and cleans the eggs. As reported for marine prawns, males and non-ovigerous females of M. amazonicum lost approximately 5% of their ingested energy in exuviae. The physiological differences observed between the sexes and between females of different reproductive stages might reflect corresponding differences in patterns of activity, growth, and reproduction.     

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.     

Maternal yolk androgens stimulate territorial behaviour in black-headed gull chicks

Avian eggs contain substantial amounts of maternal androgens. The concentrations of these yolk androgens are affected by the maternal environment, such as the level of social competition, parasite exposure or food conditions. Since yolk androgens have been shown to affect a wide array of offspring traits, they may adjust the chicks to the expected post-hatching environment, but experimental evidence is still scarce. We investigate in colonial breeding black-headed gulls whether high concentrations of yolk androgens, such as those found in environments with high numbers of social interactions, facilitate aggressiveness and territorial behaviour of the chicks. Black-headed gulls are highly suitable for this, as the semi-precocial chicks defend the natal territory and food against intruders. We manipulated yolk androgen concentrations and investigated their role in both within-nest and between-nest aggression. We found that chicks hatching from androgen-treated eggs defended the natal territory more often than their nest mates from control eggs, without increasing sibling aggression. This suggests that variation in yolk androgen concentrations in relation to the social environment of the mother may indeed allow adjustment of the offspring''s behaviour to the expected frequency of territorial interactions with conspecifics post-hatching.     

Intra- and interspecific aggression do not modulate androgen levels in dusky gregories,yet male aggression is reduced by an androgen blocker

Discussions about social behavior are generally limited to fitness effects of interactions occurring between conspecifics. However, many fitness relevant interactions take place between individuals belonging to different species. Our detailed knowledge about the role of hormones in intraspecific interactions provides a starting point to investigate how far interspecific interactions are governed by the same physiological mechanisms. Here, we carried out standardized resident–intruder (sRI) tests in the laboratory to investigate the relationship between androgens and both intra- and interspecific aggression in a year-round territorial coral reef fish, the dusky gregory, Stegastes nigricans. This damselfish species fiercely defend cultivated algal crops, used as a food source, against a broad array of species, mainly food competitors, and thus represent an ideal model system for comparisons of intra-and interspecific territorial aggression. In a first experiment, resident S. nigricans showed elevated territorial aggression against intra- and interspecific intruders, yet neither elicited a significant increase in androgen levels. However, in a second experiment where we treated residents with flutamide, an androgen receptor blocker, males but not females showed decreased aggression, both towards intra- and interspecific intruders. Thus androgens appear to affect aggression in a broader territorial context where species identity of the intruder appears to play no role. This supports the idea that the same hormonal mechanism may be relevant in intra- and interspecific interactions. We further propose that in such a case, where physiological mechanisms of behavioral responses are found to be context dependent, interspecific territorial aggression should be considered a social behavior.     

Effect of salinity on the embryonic development of Macrobrachium acanthurus (Decapoda: Palaemonidae)

The effect of salinity level on the embryonic development of Macrobrachium acanthurus was analyzed under laboratory conditions, considering characteristics of the egg (size, volume, and water content) and of the embryo (eye index). The experimental design was completely randomized, with five repetitions (ovigerous females) per treatment (0, 10, 17 and 20 ppt). During embryonic development, two eggs per female were taken daily for analyses of size, volume, water content, and eye index. Our results showed that salinity of 20 ppt leads to death and/or abortion of the embryo in all females. The size, volume and water content of eggs increased according to embryonic development, providing space in the egg for formation and organization of embryo. Salinity affected these egg characteristics, causing water loss to the hypertonic medium. Neither the duration of embryonic development nor embryo formation were affected by saltwater content. The results of the present study indicate that ovigerous females of M. acanthurus can survive in freshwater rivers as well as in low-salinity environments during incubation period and the successful larval development is not likely to rely on female migrating to estuaries. Larvae can easily be incubated in freshwater and complete development at higher salinities after hatch.     

Can reproductive traits help to explain the coexistence of mud crabs Panopeus (Decapoda: Panopeidae)? A case of two sympatric species inhabiting an impacted mangrove area of Southern Brazil

Coexistence among species is commonly related to niche divergence. However, congenerics usually are very similar in their microhabitat selection and food consumption. Thus, divergent life history strategies may represent the mechanism that allows sympatry in related species. Here, we describe and compare reproductive features in two sympatric mud crabs Panopeus americanus and P. occidentalis in an impacted mangrove area in Southern Brazil. As these species are ecologically similar, we hypothesize that these species diverge in their reproductive traits, which could explain their coexistence. Crabs were collected every two months from September 2004 to July 2006. Reproductive features such as number and size of ovigerous females, breeding season, fecundity, reproductive output, and embryo volume were assessed. Panopeus americanus produced embryos during the entire sampled period, while P. occidentalis produced only between September and March. Panopeus americanus produced more embryos considering the size of the species, had significantly lower embryo volume, and higher reproductive output than P. occidentalis. These data permit to classify P. americanus as an r-strategist and P. occidentalis as a K-strategist regarding their reproductive traits. In conclusion, our results support the hypothesis that divergent reproductive features may allow coexistence of these mud crabs.     

Shelter competition between resident male red swamp crayfish Procambarus clarkii (Girard) and conspecific intruders varying by sex and reproductive status

The shelter defense dynamics of reproductively active (Form I) male red swamp crayfish Procambarus clarkii (Girard) were investigated by staging serial intrusions by male, maternal or non-maternal female conspecifics after one day of residence. The male residents showed a direct contest advantage only against non-maternal females, and won a significantly higher proportion of the encounters against non-maternal females than against either male or maternal female intruders. However, there was no significant difference in success against male or maternal female intruders. Further experiments against male intruders showed that increasing male prior residence to either 2 or 4 days did not significantly improve the residents’ proportion of successful encounters. A final experiment revealed extremely low shelter fidelity in male P. clarkii, the most likely reason why male shelter defense against conspecific males and maternal females is not successful. These results, combined with those of past research, suggest that non-maternal females, juveniles and recently molted conspecifics are most vulnerable to predation and cannibalism, since males and maternal females easily out-compete non-maternal females for shelter, and adults out-compete juveniles. These findings may have implications for P. clarkii aquaculture and general management.     

Demography of a population of Moina micrura kurz (Crustacea: Cladocera) in a temporary pond,peninsula of paraguaná, Venezuela

A population of M. micrura Kurz from a shallow, muddy and temporary pond, located in Peninsula of Paraguaná, western Venezuela, was studied from filling to drying phase. Population density, age structure, fecundity, and length of females, were determined. This population showed a low population density (< 50 ind/1), a low and density-dependent fecundity (mean eggs/adults = 1.3; mean clutch size = 2.1 eggs + embryos), and low juveniles to adults ratio (0.71). No significant correlation was detected between mean clutch size and mean body length of ovigerous females. Our results suggest effects of food limitations, and fish predation on demographic parameters of this population. Still, in unfavourable conditions, some demographics features associated to opportunistic species were evident.     

Maternal care in the rockpool amphipod Apherusa jurinei: developmental and environmental cues

There is evidence that active, pre-emergence maternal brood care in amphipod crustaceans may be associated with ‘harsh’ environmental conditions. We examined, in the rockpool amphipod Apherusa jurinei, behavioural activities that may function as a form of active brood care. Only ovigerous females showed ‘curl’ and ‘stretch’ activities, with consequent flushing of the brood pouch and cycling of the eggs therein. There was a significant decline in these activities as embryonic development advanced and brood care almost ceased when well-developed embryos showed a heart pulse and self-ventilation. We propose that this pattern of brood care reflects changes in the physiological requirements of embryos as they develop within the egg membrane. In addition, ovigerous females showed significantly higher levels of brood care under lowered oxygen conditions. They achieved this by increasing the average duration of the ‘stretch’ component, with other brood care components remaining constant. Thus, developmental and environmental cues alter the components of active brood care in distinct ways. Experimental removal showed that the physical presence of eggs in the brood pouch is important in controlling the expression of brood care activities. However, females with all of their eggs removed continued to brood at low levels, suggesting that a maternal state also controls brood care. The sophisticated expression of active maternal brood care in amphipods under ‘harsh’ environmental conditions such as rockpools has implications both for individual reproductive success and the distribution and abundance of brooding versus nonbrooding species. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour