Paternity assurance by “helpful” males: adaptations to sperm competition in burying beetles

Summary Male burying beetles invest parentally by participating in the burial of a carcass and in provisioning and guarding the larvae that come to the carcass. Since most of the females arriving at a carcass have stored fertile sperm within their spermathecae, sperm transferred by such helpful males must compete with other males' ejaculates for the fertilization of the female's eggs. We showed that these males are able to achieve a high level of paternity (mean=92%). The mechanism they employ is a repeat-mating tactic, i.e., the female is mated very frequently shortly before and during oviposition. Repeated matings are essential for a high reliability of paternity, since single copulations result in the fertilization of only a very small proportion of the female's eggs.     

Direct and indirect estimates of sperm precedence and displacement in the dragonfly Sympetrum danae (Odonata: Libellulidae)

Summary The non-territorial dragonfly Sympetrum danae shows a high degree of post-copulatory mate-guarding, which suggests precedence of the last male's sperm. Irradiated male techniques revealed that the last male that mates with a female fertilizes an average of 95% (100% in 28% of the cases) of the clutch laid immediately after copulation, irrespective of any previous matings. Sperm volume estimates in both sexes and sperm opacity changes in females at 7 stages of copulation and oviposition indicated that males remove 41–87% of previously deposited sperm from the female's storage organs during the first 5 min of the copulation. Ejaculation takes place during the remaining 10–15 min. We maintain that indirect estimates of precedence in libellulids, based on sperm volume changes, always understimate reality because of the supplementing effect of a first-in, last out mechanism. Because males are skilled at achieving sperm precedence, they are forced to be good guards as well, since a risk of take-overs exists. Females are believed to benefit from contact guarding because it results in a lowered risk of male harassment and predation as well as a lower energy expenditure during oviposition.     

The effects of operational sex ratio and food deprivation on copulation duration in the water strider (Gerris remigis Say)

Summary A North American water strider, Gerris remigis (Hemiptera) copulates for prolonged periods of time, apparently beyond the time necessary for insemination (Rubenstein 1984; Wilcox 1984; Clark 1987), I tested predictions from two different hypotheses of the adaptive significance of this behavior. Manipulations of the operational sex ratio in artificial streams revealed that water striders copulate significantly longer when the sex ratio is male-biased. This result is consistent with the hypothesis that prolonged copulation functions as a type of contact mate guarding, which reduces sperm competition by preventing the female from remating prior to oviposition. The finding is also consistent with the hypothesis that copulation is prolonged to enhance female foraging efficiency. In a second experiment, sex ratio and total population density were held constant, and the period of food deprivation of females was manipulated. Contrary to the predictions of the female foraging hypothesis, starved females did not copulate longer than fed females. Of the two hypotheses considered, only the copulatory guarding hypothesis explains both results. This does not mean, however, that there is no selective benefit from the enhanced foraging efficiency resulting from prolonged copulation. Nor does it exclude the possibility that this benefit has been necessary for the evolution of prolonged copulation in water striders.     

Temporal variation and distribution of trace metals in freshwater and fish from Calabar River, S.E. Nigeria

An investigation on the abundance and distribution of trace metals (Fe, Cu, Zn, Mn, Cr, Cd and Pb) in water, and nine species of fish samples from Calabar river was carried out in 1992. The concentrations of iron (6000–7240gl^–1), zinc (4910–7230gl^–1), and cadmium (3–7gl^–1) showed moderate pollution while those of copper (420–630gl^–1), manganese (23–48gl^–1), chromium (<10–20gl^–1) and lead (<1–10gl^–1) in water were well below WHO permissible levels. Significant seasonal changes (0.001p0.25) were obtained for iron, copper, zinc, manganese and cadmium in water. Furthermore, iron, zinc and cadmium showed statistically significant spatial changes (0.005p0.10). Of the nine fish species studied, no statistically significant relationship between body weight and the concentrations of the metals was observed. The concentrations of the metals per mean total body weight apparently decreases in the order Fe>Zn>Cu>Mn>Pb>Cd=Cr and were within the limits that were safe for consumption.     

Costs and consequences of variation in the size of ruff leks

Summary We studied 13 ruff leks in a small region on the island of Gotland (Sweden) to investigate the effect of lek size on the costs and benefits of lekking for individual males. Male ruffs occur in two behaviourally and morphologically distinct forms, independents (residents plus marginals) and satellites, whose costs and benefits we have assessed separately. These ruff leks had from 1–10 resident (territory-holding) males and were visited daily by satellites, marginals and females from 5–25 May, when most copulations occurred. We used the average number of independent males, counted during censuses taken every 5 min during 2-h observation periods at each lek, as an index of mean lek size. Per independent male, the numbers of both satellites and females increased significantly with mean lek size. Female arrival rate and attendance (total female-minutes) also increased significantly with mean lek size as did the average per capita rate of mating success for resident males (that of satellites was not quite significant). Thus, the dispersion of both of these male categories did not appear to fit an ideal free distribution with respect to mating success. In addition, the number of independent-independent fights per independent and the rate of satellite-resident dyad formation per resident increased significantly with mean lek size. These results suggest that ruffs on larger leks enjoy higher mating success than those on smaller leks but also that costs increase with lek size. We suggest that independent males distribute themselves so as to maximize their own net benefits and that this factor can account for both the occurrence of ruff leks and the variation in their size. Correspondence to: J. Höglund     

Populational distribution I: The digital simulation

This paper presents a method of investigating the distributional pattern of a biological population, using a technique of simulation. The method consists of the comparison of the empirical frequency curve of a population, obtained using the Method of Quadrats, with a simulated one, since the pattern of the simulated curve depends on the simulated distribution. An example is given.     

Environmental Accumulation of Airborne Fluorides in Romania

The nature and extent of pollution from an aluminium smelter and a fertiliser factory in Romania were studied. These are large industrial complexes, and both types of industry are known to release fluorides into the atmosphere. In grass samples collected from around the aluminium smelter, the maximum fluoride levels were found to be 4023mgkg^–1 and 162mgkg^–1 in unwashed and washed grass samples respectively, and 89mgkg^–1 in soils. For the fertiliser factory, the maximum levels in washed grasses were found to be 207mgkg^–1, and 11mgkg^–1 in the soils. In both locations, these maximum values were obtained in samples collected from within 200m of the factory limits, and compare with regional background levels of less than 10mgkg^–1 for grasses and 2mgkg^–1 for soils. The high fluoride levels of fluoride in the grasses are sufficient to give cause for concern for the effects that these could have on the local population and on grazing animals.     

Selective males and ardent females in pipefishes

Summary In the pipefishes Syngnathus typhle and Nerophis ophidion, males have been shown to limit female reproductive rate, and females to compete for access to males. Hence, these species fit the criteria for sex-role reversal. Males brood the eggs and provide the offspring with nutrients, oxygen and an osmoregulated environment. Moreover, in S. typhle both sexes prefer a larger mate when given a choice. Sexual selection theory predicts that males should be more choosy than females, and that was experimentally demonstrated in this study. We predicted that S. typhle males should be less eager to copulate than S. typhle females with an unattractive (i.e. small) mate. We measured eagerness as the time from the start of the experiment until copulation occurred. Males with unattractive partners took significantly longer to copulate than females with unattractive partners. Moreover, females invariably initiated the courtship dance, and resumed it quicker after copulation than did the males, again suggesting reproductive hesitation in males. Neither male nor female size per se was correlated with time until copulation. In N. ophidion, where we have previously shown that males prefer larger to smaller females, we found that females did not select males with regard to size. Our results are consistent both with earlier findings (males limit female reproduction and females compete for males) and with operational sex ratios in nature: in seven annual field samples in June, the numbers of S. typhle females with ripe eggs always significantly exceeded numbers of receptive males. Hence, the potential cost of being choosy in terms of lost matings is much higher in females than in males. In conclusion, S. typhle females were somewhat choosy, but less so than males, whereas N. ophidion females were not choosy at all. Correspondence to: A. Berglund     

Male capacity as related to sperm production,pregnancy initiation,and sperm competition in deer mice (Peromyscus maniculatus)

Summary Limitations on male capacity may be important to the evolution of mating strategies and behavior. Sperm counts in successive ejaculates of deer mice (Peromyscus maniculatus) decreased progressively through six ejaculations and remained depressed the following day. Males were as effective in inseminating females in cycling estrus with their second two ejaculates as with their first two and as effective in inseminating postpartum females with their fifth as with their first. In sperm competition situations males competed with rested males as effectively with their fourth, fifth, and sixth ejaculates as with their first. Thus, although sperm counts decrease in successive ejaculates, males suffer no apparent functional deficiency as long as they continue ejaculating. It is not clear whether or not deer mice are honest salesmen but they appear to be honest ejaculators and usually are honest intromitters.     

Soil Lead at Elementary Public Schools: Comparison Between School Properties and Residential Neighbourhoods of New Orleans

Soil studies, conducted in Maryland, Minnesota and Louisiana, have described the urban pattern of lead contamination. They have shown that the highest amounts of lead cluster within the interior of the largest cities. The results of the New Orleans urban patterns of distribution of soil lead provided the basis for further study. The hypothesis was tested that elementary school properties have the same pattern of soil lead contamination as their neighbouring residential communities. Thirty New Orleans Public Elementary Schools were selected for this study. Surface samples (2.5cm or 1 inch depth) were collected from playgrounds and next to entrances of each school. Results showed that soil lead on school properties follows the same relative contamination patterns (pvalue10^–5) as soil lead on residential properties of neighbouring communities. Schools however, have significantly lower lead contamination than the neighbouring residential properties. Innercity school properties present a higher risk of soil lead exposure than mid and outercity schools. Soils next to innercity school entrances showed the highest lead, with 18.5% having concentrations over 400gg^–1. Systematic landscaping around the school entrances would significantly reduce the hazard from lead dust contaminated soils.     

Lead and cadmium in urban allotment and garden soils and vegetables in the United Kingdom

In order to assess the intake of lead and cadmium by consumers of home grown vegetables in urban areas, replicated experimental plots of uniform size, comprising summer and winter crops, were established in 94 gardens and allotments in nine towns and cities in England.The geometric mean lead and cadmium concentrations for the soils (n = 94) were 217 g g^–1 (ranging from 27 to 1,676 g g^–1) and 0.53 g g^–1 (<0.2–5.9 g g^–1), respectively. Compared with agricultural soils, the garden and allotment soils contained elevated levels of lead but not cadmium.Lead concentrations in the vegetables ranged from <0.25 g g^–1 to 16.7 g g^–1 dry weight and cadmium concentrations ranged from <0.025 g g^–1 to 10.4 g g^–1 dry weight. Lead concentrations were higher than reported background levels, although <1% exceeded the statutory limit for saleable food in the UK (1 g g^–1 fresh weight). Cadmium concentrations were generally similar to background levels.     

Reproductive biology of commercially exploited deep-water royal red prawns (Haliporoides sibogae,Solenoceridae) in south-east Australia

Deep-water royal red prawns (Haliporoides sibogae de Man, 1907; Solenoceridae: Penaeidea) were sampled from commercial catches off south-east Australia between November 1988 and May 1990. Four stages of sexual development were distinguished macroscopically for each sex. For the females, histology and analysis of oocyte size were used to validate the macroscopic staging of ovaries into undeveloped, developing, early ripe and ripe. Females were larger than males, reaching a maximum size of 46 mm carapace length (CL) compared to 32 mm CL for males. Average size at sexual maturity was 30.8 mm CL for females and 25.8 mm CL for males. Females apparently breed several times in their life, whereas males probably breed only once. Individual fecundity (ranging from about 58 000 to 140 000 oocytes) was relatively low compared with other penaeids, but oocytes were larger (mean diameter=0.41 mm). Two short breeding seasons occurred per year (February to April and July to August). There was a clear size-related latitudinal distribution of the prawns, with largr prawns (spawners) being more abundant in the northern region of the fishing area, and juveniles (CL20 mm) being more abundant in the south. Most of the spawning stock probably lies outside the main fishing ground, while the fishery targets mainly prawns below the size at maturity.     

Variation in copulation duration in Mnais pruinosa pruinosa Selys (Odonata: Calopterygidae)

Summary The Japanese calopterygid damselfly Mnais pruinosa pruinosa shows three distinct copulation durations (Siva-Jothy and Tsubaki 1989). A variety of factors which might influence copulation duration were investigated. Results indicate that the temperature in the vicinity of copulating pairs, the rate at which males encountered receptive females, territory quality, the rate of agonistic interactions between males, female gravidity and female willingness to oviposit have no effect on copulation duration. The most significant factor was the location of the site at which males captured their mates. We suggest that under natural conditions the location of the capture site provides males with reliable, indirect information about a female's intention to oviposit: it is important for males of this species to acquire such information since sperm precedence, and therefore reproductive success, is in part dependant on the interval experienced by females between copulation and subsequent oviposition. The results are discussed and it is suggested that the three observed mate-securing tactics of M.p. pruinosa are facultative and information-dependant.     

The mating system of two hybridizing species of water striders (Gerridae)

Summary We studied oviposition, feeding and mating behavior of the water striders Limnoporus dissortis and L. notabilis in sympatric and allopatric populations occurring on semi-permanent ponds in Alberta and British Columbia, Canada. Here we describe the mating system of the species and consider the evolution and maintenance of reproductive strategies employed by both sexes. Females of both species oviposited along edges of floating vegetation, either with a guarding, postcopulatory male in attendance, or alone and independent of copulation. Some females ovipositing alone were discovered by males, and when pressed for copulation, either (1) abandoned oviposition or (2) copulated and then resumed oviposition. Females that oviposited with a guarding male laid more eggs than those that completed oviposition alone. Most breeding females accepted prey offered experimentally, while a large proportion of males rejected prey but responded to model gerrids with aggressive displays and mating behavior. Males displayed three mating tactics: (1) territorial-signaling (TS), (2) patrol-signaling (PS), and (3) silent patrolling (SP). All territorial males produced surface waves from oviposition sites before attempting to mate. Some patrolling males signaled, while approaching potential mates as an aid in sex discrimination, but others did not signal and mounted both males and females. When presented with dead gerrid models, males of L. notabilis discriminated between sexes while those of L. dissortis mounted both male and female conspecifics. Collectively, males employing TS tactics fertilized more eggs than patrolling males and TS males of L. notabilis fertilized relatively more eggs than those of L. dissortis. Individual males switched frequently between territorial and patrolling behavior both under natural conditions and in field exclosures. TS males gave more signals per encounter than PS males suggesting that signaling varies with male dominance. Choice of tactic did not depend upon hunger level and was not associated with significant differences in body length in single-species populations. However, in a mixed population, the smaller males of L. dissortis were rarely territorial and signaled infrequently.     

Parental care of nestlings by male red-winged blackbirds

Summary Nestling feeding by males is less common among birds with polygynous mating systems than in monogamous species, because of the pronounced trade-off between parental behavior and the attraction of additional mates. In this study, however, we found that male red-winged blackbirds (Agelaius phoeniceus) commonly assisted females in feeding nestlings in several Ontario marshes. Male parental care was additional to that provided by females, and it significantly enhanced the fledging success of nests (Table 2). Male redwings did not help to feed all nests on their territories: primary and secondary nests were much more likely to receive male parental care than tertiary and later nests. Contrary to expectation, male parental care was not restricted to the nests of primary females: a greater proportion of secondary than primary nests were assisted (Tables 4a and b). The presence of new females settling on the territory at the same time that a resident female had nestlings, resulted in males deferring parental care until a later brood. This suggests that males trade off the recruitment of females against parental care to an existing brood. Although the number of nestlings fledging from a male's territory was strongly influenced by the number of females in the harem, males could additionally increase their reproductive success by feeding nestlings in one or more nests on their territories (Fig. 2). The reproductive success of females was significantly enhanced by male assistance in feeding nestlings (Table 3). However, those females not receiving male assistance on territories of feeding males did not suffer a significantly reduced reproductive success in comparison to females on territories of non-feeding males (Table 2). Males varied considerably in the quality of brood care given. We therefore suggest that the quality of male parental care may be a factor considered by females in choosing a breeding situation.     

Underwater oviposition in a damselfly (Odonata: Coenagrionidae) favors male vigilance,and multiple mating by females

Summary Female Enallagma hageni oviposit underwater where they are inaccessible to males. I demonstrate that males guard submerged females rather than perch sites, and are behaviorally distinct from lone males at the water. In contrast to lone males, which always attempt to copulate with females presented to them, guarding males exhibit a conditional latency to remating which corresponds closely to the time required by females to oviposit a complete clutch of eggs. By ovipositing underwater, females decrease the risk that their eggs become exposed. Risks associated with submerged oviposition favor both mate guarding, and multiple, within-clutch matings by females. Both guarding mates and lone males rescue females that float on the water surface as the result of improper resurfacing. Such behavior reduces the mortality risk to females from 0.06 to 0.02 per oviposition bout. By remating between bouts, females benefit from the additional vigilance of lone males, who rescue floating females 1.4 times as often as original mates. A second consequence of multiple mating is an increase in the selective advantage of vigilance by mates. Because receptive females become scarce by early afternoon, whereas male density remains high, a male has little (3%) chance of encountering a second receptive female that day. However, he incurs a 42% risk of losing fertilizations if he abandons a mate. For male E. hageni mate guarding functions in the context of both natural and sexual selection. It insures that a mate lives to lay a complete egg clutch in addition to protecting a male's sperm investment.     

Effect of daylight variations on the energy budgets of shallow-water corals

Energy budgets were determined for small pieces (nubbins) of the coralsPocillopora damicornis, Montipora verrucosa andPorites lobata living at a water depth of 3 m on the fringing reef of Coconut Island, Kaneohe, Hawaii. The budgets were determined for three different types of day: an ideal day with no cloud and an in situ daily integrated irradiance at 3 m of 14.385 E m^–2 d^–1; a normal day with sporadic cloud cover and daily irradiance of 11.915 E m^–2 d^–1; and an overcast day with daily irradiance of 6.128 E m^–2 d^–1. On the ideal day, the energy fixed in photosynthesis was more than that required for respiration and growth of both zooxanthellae and animal components of the association, and there was a predicted loss of between 19.3 and 32.4% of the energy fixed. On a normal day, the total photosynthetic energy fixation was lower and the excess was between 12.1 and 27.9% of the energy fixed. On the overcast day, however, in bothPocillopora damicornis andPorites lobata energy expenditure exceeded photosynthetic energy fixation and the budget was in deficit. Estimates of rate of mucus secretion on an overcast day were derived and, when incorporated into the energy budget, it was predicted that all three species would have a deficit budget, necessitating the catabolism of lipid reserves. From published values for lipid storage in these species it was calculated that the reserves would last from 28 d inPocillopora damicornis to 114 d inM. verrucosa. A model is suggested in which corals draw upon their extensive lipid stores on days of sub-optimal light, replenishing the reserves again when daily light levels are high, and finally excreting the excess energy fixed, as mucus-lipid when the lipid stores are replete.     

Why do male Callosobruchus maculatus beetles inseminate so many sperm?

Male Callosobruchus maculatus F. (Coleoptera: Bruchidae) inseminate more sperm than females can effectively store in their spermathecae. This study examines the adaptive significance of excess sperm transfer by measuring components of male and female reproductive success in response to manipulating the number of sperm inseminated. The number of sperm transferred during copulation was reduced from 56,000 ±4,462 to 8,700±1,194 by sequentially mating males to virgin females. Reducing the number of sperm inseminated by the first male to mate had no effect on the extent of sperm precedence, but reducing the number of sperm inseminated by the second male resulted in a significant reduction in the extent of sperm precedence. When large numbers of sperm are inseminated the remating refractory period of females is increased. These results indicate that males transferring large numbers of sperm during copulation have a two-fold advantage at fertilization; they are more effective at preempting previously stored sperm and they are likely to father more offspring by delaying the time of female remating. The transfer of excess sperm does not appear to serve as nonpromiscuous male mating effort; the number of eggs laid, their fertility and the subsequent survival of zygotes were unaffected by manipulating the number of sperm inseminated. The underlying mechanisms of sperm precedence were also examined. Simple models of sperm displacement failed to accurately predict the patterns of sperm precedence observed in this species. However, the results do not provide conclusive evidence against the models but rather serve to highlight our limited understanding of the movement of sperm within the female's reproductive tract.     

Female-enhanced male competition determines the first mate and principal sire in the spider Linyphia litigiosa (Linyphiidae)

Summary Two to five days before sexual maturation, female sierra dome spiders (Linyphia litigiosa: Linyphiidae) undergo a transformation in their behavior toward males that visit their webs. During this latter part of their penultimate instar, females change from consistently positioning themselves far away from males to actively maintaining close proximity, reactions I call avoidant and associative behavior, respectively. Consistent associative behavior ceases after the female's first mating and thus is limited to soon-to-mature penultimate females. When a mate-seeking male fords an associative female, he attempts to guard her until she matures; this is often a multi-day affair. In contrast, males guard immature avoidant and mature mated females for only a single day. This dichotomy in male guarding times can be understood by the fact that associative behavior signals that the female will soon develop peak reproductive value. Upon completion of their final molt, 98% of females immediately mate with the current guarding male. Secondary suitors are not as likely to achieve mating. Moreover, first mates father 1.8 times more offspring, on average, than secondary mates. Whenever they meet on any female's web, males fight until one of the contestants withdraws. Fights typically are intensive, occasionally deadly, and often result in usurpation of the web by the newly arriving male. Larger males win more fights, but other qualities (e.g., vigor and persistence) appear to be important when contestants differ by less than 10–20% in body weight. Prolonged (i.e., multi-day) guarding of associative females enhances the intrasexual selection process by ensuring that every male that arrives at the web finds it already guarded. Therefore every male that finds the web becomes a participant in a series of male-male conflicts and web usurpations which span the period between the resident female's commencement of associative behavior and her sexual maturation. Since unforced male departures from the webs of associative females are rare, victors are retained on the web until they themselves lose a fight. This facilitates a steady increase in the fighting ability of sequential guards throughout the associative period, up until female maturation and mating. On my study site, first mates represented the final winners in a combative sorting process based on a minimum average of 2 fights; they were heavier and larger than secondary mates and randomly sampled males. The combination of (1) associative behavior by nearly mature females, (2) high mating propensity of newly mature females, and (3) first male sperm priority, constitutes a system whereby females enhance male-male competition and boost the expected fighting prowess of the principal sire of their progeny. Since males appear to make no material contribution toward progeny, the female's behavior probably functions to improve the genetic constitution of the offspring. In addition, the timing of associative behavior may limit prolonged guarding by food-stealing males to a period (1) encompassing the female's pre-molt fast and (2) before the heavy yolking of eggs, thereby ameliorating the nutritional costs of intrasexual selection.     

Alternative mating tactics and the law of Diminishing Returns: The Satellite Threshold Model

Summary The mating systems of many species comprise at least 2 alternative male mating tactics — broadly termed Dominant and Satellite tactics here. But, there exists no satisfactory conceptual framework in which to explain their co-occurrence and persistence.A Dominant male's ability to copulate is a positive, but decelerating, function of either his territory's attractiveness or his own attractiveness to females. This Diminishing Returns Effect affords mating opportunities for Satellite males associated with the most attractive sites (or males). A graphical Satellite Threshold Model, analogous to the Polygyny Threshold Model (Orians 1969), is developed to predict quantitatively the presence or absence of Satellite male tactics.Five predictions of the Model are supported quantitatively by data from dragonfly and anuran social systems and, more generally, by evidence from a wide variety of species.The Model should apply both to circumstances in which males are able to alternate between tactics and the instances in which males make an irrevocable tactical decision.