Female Barbary macaque (Macaca sylvanus) copulation calls do not reveal the fertile phase but influence mating outcome

In a number of primate species, females utter loud and distinctive calls during mating. Here we aim to clarify the information content and function of Barbary macaque (Macaca sylvanus) copulation calls by testing (i) whether or not copulation calls advertise the female fertile phase and (ii) whether and how copulation calls influence male ejaculatory behaviour. In order to do this, we combined hormone measurements with acoustic analysis and behavioural observations. In contrast to a previous study implying that the structure of copulation calls indicates the timing of the fertile phase, our results, using objective endocrine criteria for assessing ovulation, provide evidence that the structure of copulation calls of female Barbary macaques does not reveal the timing of the fertile phase. More importantly, females seem to influence the likelihood of ejaculation by calling versus remaining silent and by adjusting the timing of call onset. Females make use of this ability to influence mating outcome to ensure ejaculatory matings with almost all males in the group. In addition, calls given during ejaculatory copulations differ from those during non-ejaculatory copulations, providing information about mating outcome for listeners. We conclude that in this species, copulation calls apparently serve to enhance sperm competition and maximize paternity confusion.     

Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

Although female catarrhine primates show cyclic changes in sexual behavior and sexual swellings, the value of these sexual signals in providing information to males about timing of the fertile phase is largely unclear. Recently, we have shown that in Barbary macaques, males receive information from females which enables them to discern the fertile phase and to focus their reproductive effort accordingly. Here, we investigate the nature of the cues being used by examining female sexual behavior and the size of sexual swelling as potential indicators of the fertile phase. We collected behavioral data and quantified swelling size using digital images of 11 females of the Gibraltar Barbary macaque population and related the data to the time of ovulation and the fertile phase as determined from fecal hormone analysis. We found that rates of female sexual behaviors were not correlated with female estrogen levels and did not significantly differ between the fertile and non-fertile phases of the cycle. In contrast, swelling size was significantly correlated with female estrogen levels and increased predictably towards ovulation with size being maximal during the fertile phase. Moreover, frequencies of male ejaculatory copulations showed a strong positive correlation with swelling size and highest rates were found during maximum swelling. Our data provide strong evidence that female Barbary macaques honestly signal the probability of fertility through sexual swelling and that males apparently use this information to time their mating activities. Honest advertising of the fertile phase might be part of a female strategy to manipulate male mating behavior for their own advantage, such as ensure fertilization with high quality sperm or influence paternity outcome.     

Male mating strategies and reproductive constraints in a group of wild tufted capuchin monkeys (Cebus apella nigritus)

Tufted capuchin monkeys (Cebus apella) provide an extreme example of active female sexual solicitation of males. In spite of being targeted by females for sex, males may delay copulation for hours or days. Data were collected on the sexual interactions in one wild capuchin group at the Estação Biológica de Caratinga in Brazil from September 1996 to August 1997. All successful conceptions during this year occurred in the dry season, yet sexual behavior was observed during 9 months of the year. This study tested whether male sexual response to female proceptivity was seasonally‐mediated. Male consortship participation, solicitation of females, latency to copulation, and copulation frequency were compared between fertile and nonconceptive females. Seasonal patterns in copulation interference, mating style, and alternative mating strategies were also examined. Thirty‐two copulations were observed. The alpha male was solicited for significantly more consortship days per female, but his mating success, in terms of copulation frequency, did not differ from that of two other adult males in the group. In the dry season, when the females were fertile, the males showed increased contest competition for mates, a higher frequency of alternative mating strategies against copulation interference, and increased monitoring of the females' condition. However, contrary to expectations, the alpha male's latency to copulation was significantly longer in the fertile season than in the nonconceptive months, and no males were observed to mate more than one time per day, even at the conceptive peak. Male mating strategies were affected by both season and rank, and there was evidence for reproductive constraints on males throughout the year. Limited male ejaculatory capacity and male choice in the timing of copulations within female proceptive phases may both be important factors in driving the sexual dynamics of this species. Am. J. Primatol. 67:313–328, 2005. © 2005 Wiley‐Liss, Inc.     

Sexual behavior of wild Barbary macaque males (Macaca sylvanus)

Recent assertions that the Barbary macaque (Macaca sylvanus) is a multiple-or serial-mounting species are incorrect. Data are presented from over 300 copulations observed among wild Moroccan Barbary macaques which establish empirically that males of this macaque species are single mounters. The average length of an ejaculatory copulation was 8.7 sec, with a range of 6 to 14 sec. Ejaculation occurred an average of 6.3 sec after mounting, with an average of nine pelvic thrusts per ejaculation. Males appeared capable of ejaculating twice within 16 min, and three consecutive times within 37 min. Characteristically, only one mount and ejaculation occurred during a sexual association between an estrous female and each of her consorting males. Schemes of macaque evolution which incorrectly classify Barbary macaques as a multiple-mounting species should be viewed cautiously.     

Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata)

Japanese macaques live in multi‐male/multi‐female social groups in which competition between males, female mate choice, and alternative male mating strategies are important determinants of mating and reproductive success. However, the extent to which adult males rely on female behavior to make their mating decisions as well as the effect of social rank on mating success are not clear as results are inconclusive, varying from study to study. In this study, we combined behavioral and endocrine data of 14 female Japanese macaques to examine the relationship between ovarian cycle phase and frequency of sexual behaviors, and to investigate how social rank influences sexual behavior in this species. We found that there was no increase in female proceptive behaviors during the fertile phase of the ovarian cycle, suggesting that female behaviors did not clearly signal the probability of conception. In spite of that, the frequencies of ejaculatory copulations were highest during this phase, indicating that the attractivity of females increased significantly during the period with higher probability of conception. Males, and especially the highest ranking male, were able to discriminate females nearing ovulation and to concentrate their mating effort, implying that the timing of ovulation was not concealed from them. The α male seemed able to monopolize most female matings, which is probably due in part to the low number of females simultaneously ovulating and to the limited number of inconspicuous places that the lower ranking males have to mate with females and avoid α male aggression. All together, these results suggest that different males may have access to different signals of ovulation and/or are differentially restrained as to how they can act on that information. The exact nature of the estrogen‐related cues males use to recognize female reproductive status, and to what extent males use them warrants further investigation. Am. J. Primatol. 71:868–879, 2009. © 2009 Wiley‐Liss, Inc.     

Estrogen and Progestogen Correlates of the Structure of Female Copulation Calls in Semi-Free-Ranging Barbary Macaques (<Emphasis Type="BoldItalic">Macaca sylvanus</Emphasis>)

Females of many Old World primates produce conspicuous vocalizations in combination with copulations. Indirect evidence exists that in Barbary macaques (Macaca sylvanus), the structure of these copulation calls is related to changes in reproductive hormone levels. However, the structure of these calls does not vary significantly around the timing of ovulation when estrogen and progestogen levels show marked changes. We here aimed to clarify this paradox by investigating how the steroid hormones estrogen and progesterone are related to changes in the acoustic structure of copulation calls. We collected data on semi-free-ranging Barbary macaques in Gibraltar and at La Forêt des Singes in Rocamadour, France. We determined estrogen and progestogen concentrations from fecal samples and combined them with a fine-grained structural analysis of female copulation calls (N = 775 calls of 11 females). Our analysis indicates a time lag of 3 d between changes in fecal hormone levels, adjusted for the excretion lag time, and in the acoustic structure of copulation calls. Specifically, we found that estrogen increased the duration and frequency of the calls, whereas progestogen had an antagonistic effect. Importantly, however, variation in acoustic variables did not track short-term changes such as the peak in estrogen occurring around the timing of ovulation. Taken together, our results help to explain why female Barbary macaque copulation calls are related to changes in hormone levels but fail to indicate the fertile phase.     

The function of Barbary macaque copulation calls.

In a wide variety of animal species, females produce vocalizations specific to mating contexts. It has been proposed that these copulation calls function to incite males to compete for access to the calling female. Two separate advantages of inciting male-male competition in this way have been put forward. The first suggests that as a result of calling, females are only mated by the highest ranking male in the vicinity (indirect mate choice hypothesis). The second proposes that copulation calling results in a female being mated by many males, thus promoting competition at the level of sperm (sperm competition hypothesis). In this paper, I give results from the first experimental study to test these hypotheses. Playback was used to examine the function of copulation calls of female Barbary macaques (Macaca sylvanus) in Gibraltar. Although rank did not affect lone males'' likelihood of approaching copulation calls, when playbacks were given to pairs of males only the higher ranking individual approached. Moreover, females were mated significantly sooner after playback of their copulation call than after playback of a control stimulus. These results suggest that the copulation calls of female Barbary macaques play a key role in affecting patterns of male reproductive behaviour, not only providing an indirect mechanism of female choice, but also promoting sperm competition by reducing the interval between copulations. Potential fitness benefits of inciting male-male competition at these two levels are discussed.     

Soay rams target reproductive activity towards promiscuous females' optimal insemination period

Female promiscuity is thought to have resulted in the evolution of male behaviours that confer advantages in the sperm competition that ensues. In mammalian species, males can gain a post-copulatory advantage in this sperm 'raffle' by inseminating females at the optimal time relative to ovulation, leading to the prediction that males should preferentially associate and copulate with females at these times. To the best of our knowledge, we provide the first high-resolution test of this prediction using feral Soay sheep, which have a mating system characterized by male competition for access to highly promiscuous females. We find that competitive males time their mate guarding (and hence copulations) to occur close to the optimal insemination period (OIP), when females are also increasingly likely to 'cooperate' with copulation attempts. Subordinate males practice an alternative mating tactic, where they break the integrity of the consort pair and force copulations on females. The timing of these forced copulations is also targeted towards the OIP. We thus provide quantitative evidence that female promiscuity has resulted in the evolution of reproductive strategies in which males 'load' the sperm raffle by targeting their mating activity towards female OIPs, when the probability of sperm-competition success is at its greatest.     

Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions

Recent theories on primate sexual selection have paid increasing attention to the importance of reproductive strategies of females living in multimale groups. However, the extent to which females are able effectively to conceal or advertise the time of ovulation as part of these strategies remains unclear. Few studies have investigated the ability of males to discern female reproductive status under natural conditions, and none has taken into account differences in male rank, and thus ability to gain access to females or cues. We tested male assessment of a female's fertile phase under natural conditions in longtailed macaques. We used timing of mate guarding by dominant males and the response of subordinate males towards the repeated playback of a female copulation call to measure male interest in females throughout the ovarian cycle. Relating the degree of male interest to female reproductive status, as determined noninvasively by faecal hormone analysis, we found that interest in females shown by both dominant and subordinate males was strongest during and around the fertile phase. Our results also indicate that males were better able to recognize the fertile period in conception than in nonconception cycles. Furthermore, our finding of a strong positive relation between male interest and female oestrogen levels in all cycles indicates that at least some of the cues used by males to assess female reproductive status are oestrogen related.     

Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis)

In numerous primates living in mixed-sex groups, females display probabilistic cues of fertility to simultaneously concentrate paternity to dominant males while diluting it amongst others as a means to reduce the risk of infanticide and to increase male care for offspring. A few species, however, lack these cues and potentially conceal fertility from males; yet, to date, little is known about mating patterns and their underlying proximate mechanisms in such species. Here, we investigated mating activity and sexual consortships relative to female reproductive state in wild Assamese macaques (Macaca assamensis), a species where females lack prominent anogenital swellings and copulation calls. During two mating seasons (2837 contact hours) we recorded sexual and social behaviors, sexual consortships, and collected 1178 fecal samples (n = 15 females) which were analyzed for progestogen concentrations to assess female reproductive state and to determine the timing of ovulation and conception. Although mostly conceiving in their first ovarian cycle, females were sexually receptive throughout the entire 4-month mating season, and within-cycle mating frequencies were not increased during fertile phases. Dominant males did not monopolize fertile matings, and consortships by high-ranking males lasted for long periods, which were not exclusively linked to female fertile phases. Furthermore, females copulated promiscuously but not randomly, i.e. for almost every female, matings were concentrated to a certain male, irrespective of male rank. Collectively, we demonstrate that fertility is undisclosed to males. The extreme extended female sexuality facilitated by concealed fertility may allow females to create differentiated mating relationships within a promiscuous mating system. Our study provides important new insight into the plasticity of female sexuality in non-human primates.     

Female behavioral strategies during consortship in Tibetan macaques (Macaca thibetana)

Consortship has been defined as a temporary association between an adult male and an estrous/receptive female. It has been considered as male mating strategies to improve male mating success and potential reproductive success. However, the female roles have been more or less neglected, and thus, less is known about female behavioral strategies during the consortship periods. In this study, during the two consecutive mating seasons, we collected behavioral data of free‐ranging Tibetan macaques (Macaca thibetana) habituated in Mt. Huangshan, China, to investigate female behaviors when she was consorted by an adult male. The results showed that (a) females were more likely to approach and exhibit sexual solicitation to their consorting males during the consorted period, and females also exhibited less approach to their nonconsorting males; (b) females exhibited strong responses (either departed distantly or formed affiliative relationships with their consorting male partner) when their consorting males mated with rival females or showed sexual motivation toward rival females; (c) female preferences were positively correlated to the duration of consortships and the frequencies of ejaculation copulations, independent of the social ranks of their consorting male partners. Our results suggested that female strategies played much more important roles in forming and maintaining consortship than previously assumed. It provides new insight into understanding female adaptive strategies to male strategies by forming consortships in multimale–multifemale primate species when males could not identify female''s fertile phase accurately.     

Male dominance rank and reproductive success in an enclosed group of Japanese macaques: with special reference to post-conception mating

The mating behaviour and reproductive success of male Japanese macaques (Macaca fuscata) were studied in relation to the female sexual cycles, which were monitored from the plasma profiles of gonadotropins and ovarian hormones. Based on observations of the mating behaviour during four successive mating seasons and paternity identification by DNA fingerprinting in 35 out of 37 offspring born in the subsequent birth seasons, the correlations between (1) male dominance rank and timing of mating, and (2) male dominance rank and reproductive success were examined. The results may be summarized as follows. (1) The number of copulations with ejaculation by any male was positively correlated with the male dominance rank, but not with the identified numbers of offspring fathered by each male. (2) Males could not choose ovulatory females as mating partners: the number of copulations with ejaculation with females during ovulatory weeks was not related to the male's rank. Monopolized copulations in consortship were mostly observed between high-ranking males and non-lactating parous females after conception. (3) Paternity testing showed that the male copulating most frequently with a female was not the identified father in 11 out of 15 cases. Prediction of the fathers of offspring was difficult even from the number of copulations occurring at around the estimated time of ovulation. An adaptive explanation of these correlations is discussed.     

Influence of Female Copulation Calls on Male Sexual Behavior in Captive Macaca fascicularis

We investigated the function of copulation calls—vocalizations by females during mating—in captive groups of long-tailed macaques. We tested predictions of the contest-competition, sperm competition, synchronized orgasms, mate again, alpha-male notification and graded-signal hypotheses. We observed 371 copulations of 36 females wherein the presence or absence of a copulation call was clear. Females call equally often with different males and shortly after ejaculation. Copulation calls occurred equally with copulations with and without ejaculation. Calls did not incite disruptions of the mating. Following calls females mated again, more often than expected, with their mating partner. Both pregnant and fertile females uttered copulation calls. Two females conceived and mated mainly with the alpha male then. We conclude that copulation calls do not incite male contest competition for sexual access to females and that it is unlikely that calls synchronize male and female orgasms. Several hypotheses remain plausible, but not all predictions are borne out unequivocably. This alerts us to the possibility that the calls could have multiple beneficial effects; natural selection might strike a compromise among functions. Investigation of the mate again, sperm competition and alpha-male notification hypotheses, and of hypotheses not tested in our study concerning female breeding overlap and female-female agonism, is required.     

Behavioral indicators of ovarian phase in white-faced capuchins (Cebus capucinus)

In many primate species, conspicuous behavioral and/or morphological changes are indicators of the fertile phase of the female cycle. However, several primate species, such as the white-faced capuchin, lack these cues. This is referred to as "concealed ovulation," and is argued to be a reproductive strategy that confuses paternity and lowers the risk of infanticide. We studied 10 adult female white-faced capuchins in Santa Rosa National Park, Costa Rica, from January to June 2002. We determined their ovarian cycling patterns by analyzing fecal ovarian hormones, and compared simultaneously collected behavioral data to determine which, if any, cues females use to signal their fertile phases. We found that four females cycled during the study period but ceased to cycle without becoming pregnant. We considered several explanations for the lack of conception during our study, including reproductive seasonality. We found that female C. capucinus showed only small increases in rates of affiliative/proceptive behaviors directed toward adult males during their periovulatory phases. The best indicator of cycle phase was a significant increase in male affiliative behaviors (e.g., following and grooming bouts) and sexual behaviors (e.g., copulations and courtship displays) directed toward females during the periovulatory phase compared to the nonovulatory phase. Our finding that females exhibit little proceptive behavior, but that copulations and male courtship are nonetheless concentrated in periovulatory phases suggests that even though females do not provide behavioral and morphological cues to ovulation, males are still able to detect it. Infanticide occurs with some frequency in these monkeys, and there is evidence for postconceptive mating as a female strategy to lower risk of infanticide via paternity confusion. However, despite this occurrence of nonconceptive mating and the absence of female cues to ovulation, truly concealed ovulation does not appear to be characteristic of this study population of white-faced capuchins.     

Behavioural aspects of the raccoon mating system: determinants of consortship success

We monitored raccoons Procyon lotor, in southern Texas during the 1990-1992 mating seasons to describe mating behaviour and identify factors affecting consortship success. During most of this study, raccoons were spatially aggregated, with female home ranges congregated around permanent water sources and larger home ranges of male groups encompassing each female group. Consortship success varied among males and ranged from zero to six females per male within a mating season. Individual females consorted with one to four different males during an oestrous period; however, most (62%) females consorted with only one male during their oestrus. Dominance through overt conflict appeared to influence male consortship success. During two mating seasons, one male from each group consorted with females on more days than all other males combined. Body weight of males was positively correlated with number of consortship days. As synchrony of oestrus increased, variance in number of consortship days among males decreased, and access to oestrous females increased for subordinate males. Wounding among males increased during the mating season, and was more frequent for males than for females. The mating system, as determined by consortship behaviour, appeared to shift between polygyny and promiscuity, and possibly varied annually as a result of the timing of oestrous cycles. Copyright 1999 The Association for the Study of Animal Behaviour.     

Sneaky Monkeys: An Audience Effect of Male Rhesus Macaques (Macaca mulatta) on Sexual Behavior

Males and females have different sexual interests and subsequently may show conflicting sexual strategies. While dominant males try to monopolize females, promiscuity benefits females and subordinate males. One way to escape monopolization by dominant males is to copulate in their absence. We tested this inhibitory effect of males on the sexual behavior of their group members in captive group‐living Rhesus macaques. Copulations between females and nonalpha males almost exclusively took place when the alpha male was out of sight. Furthermore, the inhibiting effect was not unique for the alpha male. An upcoming nonalpha male also inhibited copulations of its group members, and three other nonalpha males inhibited female copulation solicitations. Females adjusted their behavior to the presence of bystander males, as they initiated and accepted initiations more often in absence than in presence of bystander males. Although not significant, in males, a similar pattern was found. The observed reduction in mating behavior in presence of bystander males is in accordance with an “audience effect,” in which the behavior is modulated in relation to the presence or absence of third parties. This audience effect may serve as an important mechanism to reduce (aggressive) interruptions of subordinate male copulations.     

Female mate choice across mating stages and between sequential mates in flour beetles

Few studies have examined how female premating choice correlates with the outcome of copulatory and post-copulatory processes. It has been shown that polyandrous Tribolium castaneum females discriminate among males before mating based on olfactory cues, and also exert cryptic choice during mating through several mechanisms. This study tested whether a male's relative attractiveness predicted his insemination success during copulation. Bioassays with male olfactory cues were used to rank two males as more and less attractive to females; each female was then mated to either her more attractive male followed by less attractive male, or vice versa. Dissections immediately after second copulations revealed a significantly higher percent of successful inseminations for females that remated with more attractive males compared with those that remated with less attractive males. These results indicate that cryptic female choice during copulation reinforces precopulatory female choice in T. castaneum, and suggest that females could use cryptic choice to trade up to more attractive males, possibly gaining better phenotypic or genetic quality of sires.     

Post-conception mating in wild long-tailed macaques (Macaca fascicularis): characterization, endocrine correlates and functional significance

In many anthropoid primates, mating activity is not restricted to the ovarian cycle but also occurs during pregnancy. Although it has been suggested that the main function of this post-conception mating is to confuse paternity, studies showing whether or not male primates can distinguish between the fertile phase of the conception cycle (FPCC) and the period of peak post-conception mating (peak PCM) are almost non-existent. Here, we examine whether the pattern of female sexual traits (specific sexual behaviors, sexual swelling) and female attractiveness to males differ between FPCC and peak PCM in 6 wild female long-tailed macaques. We also use fecal hormone analysis to investigate whether female traits during peak PCM are related to changes in female sex hormones. All females exhibited a distinct period of heightened mating activity around days 45-60 of gestation. During peak PCM, swelling size and frequency of female solicitations (but not reaching back) were significantly correlated with changes in the estrogen to progestogen ratio. Swelling size, frequency of female sexual behaviors and copulations and proportion of male-initiated copulations and ejaculations were not significantly different between FPCC and peak PCM. Although males spent significantly less time consorting females during peak PCM, all (particularly low-ranking and non-resident males) invested heavily in terms of reproductive costs associated with mate-guarding and mating during pregnancy. We conclude that post-conception mating in wild long-tailed macaques is not merely a by-product of endocrine changes and devoid of adaptive function. Our results more strongly support the hypothesis that it may form part of a female reproductive strategy to confuse paternity, which appears to apply particularly to low-ranking and extra-group males.     

Female reproductive signaling, and male mating behavior, in the olive baboon

Baboon sexual swellings are among the largest and most colorful signals displayed by any mammal, and many baboon studies have shown an association between sexual swellings and both female and male sexual behavior. However, the extent to which female behavior and sexual swellings combine to signal the timing of ovulation and the fertile period to males, and the extent to which males use these and other signals when determining patterns of mating behavior, remain key topics of research. Here we assess the social and sexual behavior of both female and male olive baboons with respect to detailed measures of swelling size made from digital photographs, measures of fecal progestogen and estrogen levels, and estimates of the timing of ovulation and the fertile period based on those levels. Female aggression and grooming behavior were unrelated to fecal progestogen and estrogen levels, but there were some significant relationships between these hormonal measures and presenting behaviors. Measures of female behavior collected during the study did not appear to reveal the timing of ovulation or the fertile period. Male consortship behavior was closely tied to fine-scale changes in sexual swelling size, but copulation behavior was not. Copulation behavior of consorting males was, however, linked to the timing of both ovulation and the fertile period, suggesting that males did have knowledge about these timings. Together these results suggest that males used fine-scale swelling size changes when deciding when to consort, but that consorting males did not use fine-scale swelling size changes in deciding when to copulate. We propose that swelling size may advertise the period during which males should consort with females, with other signals available only from closer inspection then used by consorting males to assess the timing of the fertile period more accurately. An important implication of this interpretation is that different males may have access to different signals of ovulation at any one time. Such a system would allow females to offer different males different information simultaneously, perhaps offering a solution to the ‘female dilemma’ of how females can simultaneously assure and confuse paternity in multi-male societies.     

Copulation patterns in captive hamadryas baboons: a quantitative analysis

For primates, as for many other vertebrates, copulation which results in ejaculation is a prerequisite for reproduction. The probability of ejaculation is affected by various physiological and social factors, for example reproductive state of male and female and operational sex-ratio. In this paper, we present quantitative and qualitative data on patterns of sexual behaviour in a captive group of hamadryas baboons (Papio hamadryas), a species with a polygynous–monandric mating system. We observed more than 700 copulations and analysed factors that can affect the probability of ejaculation. Multilevel logistic regression analysis and Akaike’s information criterion (AIC) model selection procedures revealed that the probability of successful copulation increased as the size of female sexual swellings increased, indicating increased probability of ovulation, and as the number of females per one-male unit (OMU) decreased. In contrast, occurrence of female copulation calls, sex of the copulation initiator, and previous male aggression toward females did not affect the probability of ejaculation. Synchrony of oestrus cycles also had no effect (most likely because the sample size was too small). We also observed 29 extra-group copulations by two non-adult males. Our results indicate that male hamadryas baboons copulated more successfully around the time of ovulation and that males in large OMUs with many females may be confronted by time or energy-allocation problems.