Puddling: from natural history to understanding how it affects fitness

The term ‘puddling’ includes feeding on (dried) mud and various excrements and secretions of vertebrates, and carrion. It is thought to be a form of supplementary feeding, not targeted at obtaining energy. Although the natural history of the puddling phenomenon in herbivorous arthropods becomes better known, it is still largely unclear how puddling (in particular for sodium) affects fitness despite the growing knowledge of insect physiology at the cellular level. If we follow the definition used for puddling in Lepidoptera, representatives of a wide range of herbivorous and detrivorous terrestrial arthropods (Lepidoptera, Orthoptera, Blattodea, Hymenoptera, Hemiptera, Diptera, and Diplopoda) have been observed to puddle. It appears that those species with diets low in sodium (e.g., folivorous larvae) puddle for sodium whereas those with diets low in nitrogen (e.g., detritivores) puddle for nitrogen. Sex differentials in puddling behavior can usually be explained by transfers of nutrients from males to females during mating. Puddling is rare or absent in immature stages and there is some evidence that nutrients from puddles increase female reproductive success. Strong evidence for the widely cited hypothesis that sodium from puddles is used to enhance neuromuscular activity is still lacking. High mobility and long life spans could be associated with puddling behavior, whereas insects that are concealed or well defended are less likely to puddle (e.g., beetles). The role that risks of pathogen and parasite infection as well as predation at puddling substrates may play in the evolution of puddling remains virtually unexplored.     

Puddling in butterflies: sodium affects reproductive success in Thymelicus lineola*

ABSTRACT. Adults of many species of Lepidoptera, principally the males, frequent mud puddles, edges of streams, carrion and animal excreta where they imbibe moisture, an activity referred to as 'puddling' Sodium ions are the only known stimulus present which cause males of at least two lepidopteran species to drink for extended periods. In the European skipper Thymelicus lineola (Ochsenheimer) (Lepidoptera: Hesperiidae), only males puddle, even though they have concentrations of abdominal sodium 2–3 times that of females at emergence. During their first mating, males transfer 32% of their abdominal sodium to females. This could be of considerable importance given that an average egg complement contains >50% of the total body sodium of females at emergence. Virgin females, as well as having reduced fecundity, have reduced longevity. This is attributed to virgins not obtaining important nutrients which males transfer to females during mating. Access to sodium ions increases the total number of matings by c. 50% for males living >15 days. Access to sodium ions by once-mated males increases the percentage of males which re-mate on the day following first mating; the percentage of females, mated to the twice-mated males, which lay >50% fertile eggs; and the drought resistance of eggs laid by those females.     

Unequal distribution of local mating opportunities in an egg parasitoid

Abstract.  1. The Local Mate Competition (LMC) model predicts that, in gregarious and quasi-gregarious species, a lone female exploiting a host patch will lay only the minimal number of sons necessary to inseminate all daughters, but as the number of foundresses increases, the proportion of sons deposited by these females also increases.
2. For off-patch mating to occur, non-sperm-depleted males must leave the patch and find virgin females.
3. To investigate the distribution of matings among males, the sperm stock at dispersal and the time of dispersal were quantified for male Trichogramma turkestanica (Hymenoptera: Trichogrammatidae).
4. Matings were not distributed equally among males: some successful males acquired more matings than others. Because of this, a high variability in the sperm stock at dispersal was observed. While few males dispersed almost empty or almost full, the majority of males dispersed with enough sperm to be able to mate with females outside the emergence patch.
5. The mating capacity was thus higher than necessary for local mating and could be explained by an unequal distribution of mating opportunities and the occurrence of off-patch mating.     

Assortative mating in fallow deer reduces the strength of sexual selection

Background

Assortative mating can help explain how genetic variation for male quality is maintained even in highly polygynous species. Here, we present a longitudinal study examining how female and male ages, as well as male social dominance, affect assortative mating in fallow deer (Dama dama) over 10 years. Assortative mating could help explain the substantial proportion of females that do not mate with prime-aged, high ranking males, despite very high mating skew. We investigated the temporal pattern of female and male matings, and the relationship between female age and the age and dominance of their mates.

Results

The peak of yearling female matings was four days later than the peak for older females. Younger females, and especially yearlings, mated with younger and lower-ranking males than older females. Similarly, young males and lower-ranking males mated with younger females than older males and higher-ranking males. Furthermore, the timing of matings by young males coincided with the peak of yearling female matings, whereas the timing of older male matings (irrespective of rank) coincided with the peak of older female matings.

Conclusions

Assortative mating, through a combination of indirect and/or direct female mate choice, can help explain the persistence of genetic variation for male traits associated with reproductive success.     

A life-history perspective on strategic mating effort in male scorpionflies

In species with high male mating effort, there is a trade-offbetween mating effort spent in a current mating and resourcesleft for future matings. Consequently, to maximize their reproductivesuccess, males have to invest strategically, saving resourcesin matings with low reproductive gain for future, more valuablematings. However, as males age, the expected future reproductivesuccess constantly declines. Thus, the importance of resource rationing may drastically change during a lifetime. Males ofthe scorpionfly Panorpa cognata offer females a costly nuptialgift before copulation, which functions as male mating effort.Resources for the production of these salivary masses are severelylimited for males in poor condition. We found that males investedmore in copulations with high-quality females than in copulationswith low-quality females. However, males ceased to discriminateas they became older. Old males, with a relative small numberof expected future matings, did not invest differentially incopulations with high- versus low-quality females. In copulationswith low-quality females, males invested more in late thanin initial matings, whereas in matings with high-quality females,time of mating had no influence on mating effort. These resultsimply that males adaptively change their resource allocationstrategy during the course of the season. Initial matings seemto be characterized by male prudence; in later matings, malesseem to adopt a more opportunistic mating strategy.     

Is male puddling behaviour of tropical butterflies targeted at sodium for nuptial gifts or activity?

An apparent sexual difference in adult feeding behaviour in many species of Lepidoptera relates to puddling on mud, dung and carrion. In most butterfly species, puddling is exclusively a male behaviour. A possible explanation for this division in feeding behaviour is that nutrients derived from puddling are transferred to the female in the spermatophore during mating as a nuptial gift. Sodium derived from puddling has been shown to act as a nuptial gift in a few Lepidoptera species. It can also be used for neuromuscular activity in both males and females and may therefore correlate with flight morphology. In this study, we examine the generality of these two hypotheses in comparative work on a community of African fruit-feeding butterflies. We investigated puddling behaviour of males and females on carrion and dung together with sodium preferences, polyandry, relative wing-size, sexual size dimorphism and sodium concentrations in the bodies and spermatophores of several species. The results show that sodium as a nuptial gift can explain the sexual division in puddling in some species, but not in all. Species in which both sexes puddle transfer little sodium in the nuptial gift, which is consistent with the nuptial gift theory. Wing loading and puddling are not significantly correlated, but the trend followed the direction predicted by the activity hypothesis. However, the sodium concentration in the species with the smallest wing area to thoracic volume (WA/TV) ratio (the largest Charaxes spp.), was relatively low. Moreover, in all investigated species, the sodium concentration was higher in the abdomen than in the thorax. The results are discussed in the light of differences between the sexes in foraging behaviour in both larvae and adults, and with respect to alternative explanations for puddling.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 345–361.     

Laboratory breeding studies of freshwater crayfish, Austropotamobius pallipes (Lereboullet)

SUMMARY. 1. Mature crayfish, collected from an Irish lake before breeding had started, were held in breeding combinations and their mating and brooding activities observed.
2. All mating attempts were initiated by the male. A single mating led to spawning within 6 days but a subsequent mating cancelled the effects of the first. Males mated more often when there were more females present. Males lacking a major cheliped mated less often than did normal males.
3. Larger males mated more often than did smaller males, and although males showed no female size preference, matings were less frequent and generally unsuccessful when males were much larger than females; the female was usually killed. Large females mated successfully with smaller males.
4. Females held at high densities with a larger male mated earlier than at low densities. However, aggression also increased with density; at high densities males fought and killed females.
5. Males held in pairs without females fought; in occasional mating attempts spermatophores were not positioned correctly. Paired females rarely fought; all spawned normally although unmated. Although their eggs soon died and were removed during grooming, brooding behaviour continued for at least 2 months.
6. Brooding females held in pairs shed pleopodal eggs during aggressive encounters. Females held singly showed a lower initial rate of egg loss.     

Methoprene-induced matings of young Queensland fruit fly males are effective at inducing sexual inhibition in females

Pre-release dietary treatment with methoprene, a juvenile hormone analogue, decreases the age at which male Queensland fruit flies mature and hence may decrease the post-release delay until released sterile flies participate in sterile insect technique (SIT) programmes. However, if matings of young methoprene-treated males are not effective at inducing sexual inhibition in their mates, then this treatment may not enhance SIT. The present study investigates efficacy of matings of methoprene-treated males at inducing sexual inhibition in their mates. Methoprene incorporated into a diet of sugar and yeast hydrolysate (w/w 3:1) for 48 hr after emergence resulted in significantly increased male mating propensity when flies were <10 days of age, but not when older, and longer copulations. Copula latency did not vary with methoprene treatment but did decrease with age. The matings of young methoprene-treated males were effective at inducing sexual inhibition in their mates, matching the efficacy of untreated mature males. Regardless of treatment, females had reduced tendency to remate if their first mate was 15 days of age than if their first mate was younger (6, 8 days) or older (20, 25, 30 days). Females mated by methoprene-treated males that did remate tended to remate later in the day than females mated by untreated males. Also, second copula durations of females first mated by a 6- to 10-day-old male were shorter if the male was methoprene treated. These patterns in remating females may indicate greater efficacy of the initial mating of methoprene-treated males. Overall, we find that the additional matings of young methoprene-treated male Queensland fruit flies are effective at inducing sexual inhibition in their mates. This finding supports the incorporation of methoprene into pre-release diet for SIT.     

Quantitative aspects of the effect of mating on readiness to lay in the Australian sheep blowfly,Lucilia cuprina

Virgin females of Lucilia cuprinararely lay eggs, whereas mated females do so readily. This effect of mating is due entirely to increased readiness to lay, and not to any effect on ovarian development. An investigation was made of how readiness to lay was affected by matings which differed in terms of the male's chemical and mechanical contribution. Individual males were mated, during 1 day, to a succession of females whose readiness to lay was determined 1 or 8 days after mating. On both days, the proportion of females laying was inversely related to the number of females with which the male had previously mated. A high proportion of females that had mated with previously unmated or oncemated males laid at both 1 and 8 days after mating. However, this proportion tended to decline between day 1 and day 8 in females that had mated with males with two or more previous matings, and this effect was most evident in females mated with males that had previously mated with four or more females. When matings were manually terminated as soon as coupling had occurred, the proportion laying remained as low as in virgins. This proportion progressively increased as mating duration increased from 2 to 6 min. The proportion that laid after mating terminated at 6 or 8 min was as high as that for females from full-term matings (mean duration, 12.5 min). The results are generally similar to those obtained in parallel experiments on the effect of mating on sexual receptivity in this species and, therefore, indicate that the physiological bases for the two effects of mating might be the same.     

The role of male age, sperm age and mating history on fecundity and fertilization success in the hide beetle

Models of age-related mate choice predict female preference for older males as they have proven survival ability. However, these models rarely address differences in sperm age and male mating history when evaluating the potential benefits to females from older partners. We used a novel experimental design to assess simultaneously the relative importance of these three parameters in the hide beetle, Dermestes maculatus. In a two-part experiment we first explored age-related male mating success and subsequently examined the consequences of male age, sperm age and male mating history on female fecundity and fertilization success. In a competitive mating environment, intermediate-age males gained significantly higher mating success than younger or older males. To test the consequences for females of aged-related male mating success, a second set of females were mated to males varying in age (young, intermediate-age and old), in numbers of matings and in timing of the most recent mating. We found that male age had a significant impact on female fecundity and fertilization success. Females mated to intermediate-age males laid more eggs and attained consistently higher levels of fertilization success than females with young and old mates. A male's previous mating history determined his current reproductive effort; virgin males spent longer in copula than males with prior mating opportunities. However, differences in copulation duration did not translate into increased fecundity or fertilization success. There was also little evidence to suggest that fertilization success was dependent on the age of a male's sperm. The experiment highlights the potential direct benefits accrued by females through mating with particular aged males. Such benefits are largely ignored by traditional viability models of age-related male mating success.     

Males mate with females even after sperm depletion in the two-spotted spider mite

Generally, males increase their reproductive success by mating with as many females as possible, whereas females increase their reproductive success by choosing males who provide more direct and indirect benefits. The difference in reproductive strategy between the sexes creates intense competition among males for access to females, therefore males spend much energy and time for competition with rival males for their reproduction. However, if they do not need to engage themselves into male competition and females are in no short supply, how many females can a male mate with and fertilize? We address this question in the two-spotted spider mite, Tetranychus urticae Koch. In this study, we investigated how many females a young, virgin male mated in 3 h, and checked whether the mated females were fertilized. We found that on average males mated with 12–13 females (range: 5–25). As latency to next mating did not change with the number of matings, the males are predicted to engage in even more matings if the mating trial were continued beyond 3 h. Copulation durations decreased with the number of matings and typically after 11 copulations with females any further copulations did not lead to fertilization, suggesting that males continued to mate with females even after sperm depletion. We discuss why spider mite males continue to display mating and copulation behaviour even after their sperm is depleted.

     

Reproductive strategies of Aphidius ervi Haliday (Hymenoptera: Aphidiidae)

Hymenopteran parasitoids are usually arrhenotokous parthenogenetic, where females arise from fertilized and males from unfertilized eggs. Therefore, the reproductive fitness of females is a function of egg production and furthermore affected by mating, whereas that of males is mainly determined by the number of daughters they father. Aphidius ervi Haliday is a quasi-gregarious parasitoid of a number of aphid pests on economically important crops such as legumes and cereals. Females are monandrous whereas males are polygynous. Here, we tested how parental age at mating and male mating history affected mating success, fecundity and daughter production in this species. Once-mated males perform significantly better than naïve males with regard to mating success, suggesting that males learn from previous matings. The fecundity of virgin females is not significantly different from that of mated females regardless of parental age at mating and male mating history, indicating that mating does not stimulate egg production or contribute to female nutrient supply. Males can replenish sperm supply after mating, implying that they are at least moderately synspermatogenic. Preference for young over old mates for mating by both sexes may be explained by the fact that aging of both sexes contributes to the reduction of daughter production. Rather than sperm depletion, the reduced daughter production may be attributed to diminishing sperm viability and mobility in aging males and increasing constraints in fertilization process in aging females. Our results also show that female age has a stronger impact on the production of daughters, suggesting that fertilization process in females is more sensitive to aging than sperm vigor in males.     

Reproductive behavior of the honeydew moth,Cryptoblabes gnidiella

Summary

The reproductive behavior of the honeydew moth, Cryptoblabes gnidiella (Millière) (Lepidoptera: Pyralidae), was studied in the laboratory. The sex ratio was 1.1:1, males to females, in both laboratory and field stocks. Most of the females that mated did so during the first night after emergence; males began mating on the following night. Mating occurred 1–2 h before dawn and averaged 100 min. Both sexes mated only once in one night. Most females mated only once in their lifetime, a few mated 2–4 times, whereas males mated up to six times per lifetime. Insects that lived longer also mated more times. When the sex ratio was altered from 3:1 to 1:3, males to females, the percentage of females that mated in one night dropped from 90 to 65, whereas the number of matings per male rose from 0.32 to 2.25. When fresh one-day-old females were provided daily at a ratio of three per male, the males averaged 1.4 matings per lifetime vs. 2.6 with 2- to 3-day-old females. A delay in mating did not affect the percentages of males and females that mated; highest percentages were obtained with 2- to 4-day-old males and females, but a delay in mating resulted in egg fertility dropping from 91 % to 73 %. The preoviposition period lasted a full day after mating, and then most of the eggs were laid during the first night. Average fecundity was 105 eggs per female (maximum: 230).     

Conflict resolution in the Odonata: implications for understanding female mating patterns and female choice

Predictions of mating patterns in animals have focused on males and how they compete for fertilizations by controlling females. With reference to the Odonata, a taxon in which mating requires cooperation of the female, the active role that females play in mating decisions is often ignored, leading to the premature conclusion that male coercion of females is common. A critical review of the outcome of sexual conflict among odonates leads me to alternative explanations of female mating patterns that need to be refuted before concluding that males coerce matings. Because Anisoptera males have greater control over tandem formation, they have a greater potential for coercion than Zygoptera males. However, Anisoptera females may simply be willing to remate more often if they receive insufficient sperm to fertilize an entire egg clutch. Contrary to prior assumptions, in both suborders, male defence of oviposition sites does not preclude females from choosing among sites or among males. I find that the evolution of non-aggressive sexual signals by males is a reliable indication that sexual conflict has been resolved in favour of female interests. Although I predict that the benefits to females of choice of male phenotype should rarely exceed the cost of such discrimination in Odonata, female choice is most likely to evolve in territorial species whose males must endure high physiological stress in order to mate, and when site quality is not a reliable predictor of the genetic quality of a potential mate.     

Effect of multiple mating on the reproductive performance of the rice leaffolder moth,Cnaphalocrocis medinalis (Lepidoptera: Crambidae)

To clarify whether multiple mating of females and males affects the reproductive performance of the rice leaffolder moth, Cnaphalocrocis medinalis (Guenée), we examined the effect of the number of matings (once, twice, or three times) for females (female treatment) and males (male treatment) on the incidence of moth mating, number of eggs laid, egg hatchability, and adult longevity. We also compared the effect of multiple mating imposed on males or females separately with the effect of that imposed on both sexes simultaneously (both sexes treatment). The incidence of mating of females and males that mated three times (3-mated females and males) was significantly lower than for females and males that mated twice or once (2-mated or 1-mated females and males). The incidence of mating of 1-mated moths (both sexes) was significantly higher than for 2-mated or 3-mated moths (both sexes). Two-mated or 3-mated females laid significantly more eggs with significantly higher hatchability than 1-mated females. Females that mated with 1-mated males (second male mating) or 2-mated males (third male mating) laid significantly fewer eggs than those that mated with virgin males (first male mating). Females laid significantly more eggs after the second and third matings for moths of both sexes than after the first mating for moths of both sexes. The mechanisms of improvement and decline of female reproductive performance when multiple mating was imposed on males or females are also discussed in relation to the reproductive biology of C. medinalis.     

Strategic sperm allocation in the Small White butterfly Pieris rapae (Lepidoptera: Pieridae)

1. In species where females mate multiply, it is important for males to recuperate quickly in order to maximize their fertilization success. Butterflies produce a spermatophore at mating containing accessory secretions and sperm of two types: a large number of non-fertile 'apyrene' sperm and fewer fertile 'eupyrene' sperm. Many butterfly species eclose with most nutrients for reproduction already present. Males must therefore decide how to allocate resources to the various spermatophore components at any given mating.
2. Recovery rates of apyrene and eupyrene sperm number and spermatophore size was studied in the polyandrous Small White butterfly Pieris rapae . The mass of the first spermatophore increases with time since eclosion, as does the number of both types of sperm. Similarly, on a male's second mating, both the mass of the spermatophore and the number of sperm increases with time since the first mating.
3. However, the rate of increase in eupyrene sperm numbers is higher after the first mating. The difference in rate of increase may be the result of different probabilities of virgin and non-virgin males obtaining future matings.
4. Males have a sperm storage organ, the duplex, in which they retain sperm after their first mating. This ensures that high sperm numbers are available for their second mating, even when remating only 1 h later. Thus, males do not ejaculate all available sperm on any given mating, and seem to have different strategies on their first and second matings.
5. It can be argued that Small White butterfly males allocate sperm strategically according to the probability of obtaining subsequent matings, and the level of sperm competition.     

Male age, mating status and nuptial gift quality in a bushcricket

Female mate choice occurs in many animals, and in some species females prefer older males. Because older males have demonstrated their survival ability, they may be of higher genetic quality, providing genetic benefits to the offspring of their mates. However, in species where females receive direct benefits of matings, younger males may be more likely to provide more fertile or more nutritious ejaculates, so females may discriminate against older males. Males of the bushcricket Ephippiger ephippiger (Orthoptera: Tettigoniidae) produce large spermatophores at mating (>30% of body weight, circa 10% protein content). Female E. ephippiger discriminate against the song of older males. We examined the effects of male age and mating history on male reproductive investment (spermatophore size, sperm number, nitrogen content). Males produced spermatophores with significantly fewer sperm and of lower nitrogen content on their fourth mating, despite free access to food and a 1-week interval between matings, indicating that there is a cost of mating to males. There was no indication that older virgin males produced lower-quality spermatophores. Rather, older males produced bigger spermatophores of higher nutritional value and containing more sperm. Male age and mating history seem likely to be strongly correlated in the field. We conclude that female E. ephippiger probably prefer the songs of younger males, because in the field, this preference correlates with male mating history and therefore resources provided at mating. Thus, female preference for younger males could reflect discrimination against low-quality nuptial gifts.     

Mating Behavior and Reproductive Potential in the Turnip Moth Agrotis segetum (Lepidoptera: Noctuidae)

We investigated the lifetime mating potential and the reproductive behavior of male and female turnip moths Agrotis segetum (Schiff.) under field and laboratory conditions. The sex ratio was 1 : 1 in a lab-reared population as well as in two wild populations. Males were capable of mating repetitively a relatively large number of times (mean of 6.7 ± 2.7 matings) when given access to new virgin females throughout their lifetimes. Females seldom mated more than once (mean ± 1.3 ± 0.6 matings), indicating a male-biased operational sex ratio. The mean potential lifetime mating was five times higher in males, while the coefficient of variance was lower in males. There was no differences in longevity between animals that were allowed to mate and animals not allowed to mate, indicating no direct costs or benefits of mating in physiological terms. In males, the number of matings was positively correlated with longevity, but this was not the case in females. Nor was there a correlation between the number of female matings and the number of fertilized eggs. There was a negative correlation between the number of eggs fertilized and the number of times males had previously mated, indicating that male ejaculates were limited. Male spermatophore size also decreased with number of achieved matings. Laboratory-reared females attracted males in the field throughout their lifetimes, with a peak at 3–7 days of age. Wild males, allowed to choose between pairs of caged females in the field, were attracted in equal numbers to females of different ages. Females did not show any mate-rejection behavior in the field. They mated with the first male that courted them. No incidence of mate replacement by males arriving later to already courted females were recorded.     

Opportunistic and restrictive matings among wild chimpanzees in the Mahale Mountains,Tanzania

The mating patterns of free-ranging chimpanzees (Pan troglodytes) of the Mahale Mountains, Tanzania, were studied. Opportunistic mating (non-competitive and temporary mating) was frequently observed in a large-sized unit-group, among young, low-ranking males, and among young, newcomer, non-ovulating females. Restrictive mating (a continuous sexual relationship between a particular pair which includes possessiveness and consortship) was frequently observed in a small-sized unit-group, among middle- and old-aged, high-ranking males, and among old, resident, ovulating females. Relations between those characteristics, such as group size and composition, ages of the individuals of both sexes, female estrous stages, and life history, and the 2 mating patterns are discussed.     

Sexually dimorphic growth in the dioecious tropical shrub, Siparuna grandiflora

1. To demonstrate evolved sex-based differences in vegetative traits of dioecious plant species, one must consider both pre-reproductive and reproductive individuals, as dimorphic patterns commonly arise secondarily from different effects of reproduction on resource balance.
2. Siparuna grandiflora , a neotropical dioecious shrub in which females allocate significantly more biomass to reproduction than males, was studied for 2 years (three reproductive events) to determine whether sex-based differences in stem growth, leaf production and allocation pattern could be detected in pre-reproductive individuals grown from cuttings in field plots or in mature naturally occurring individuals.
3. Among pre-reproductive individuals, females accumulated more stem and leaves than males, but among mature individuals, no sex-based growth differences were apparent. In mature individuals, both growth and leaf longevity were positively correlated with reproductive frequency. With regards allocation, pre-reproductive males had larger leaves than females, and mature females allocated less biomass per unit stem length than males.
4. The capacity of pre-reproductive females to grow faster than males demonstrates innate differences between the sexes. That mature females achieved equivalent growth to males, despite higher reproductive allocation, indicates that the greater growth capacity of young females is sustained in older females and enables them to compensate for greater reproductive allocation.