Low Reproductive Value Research Articles

Balancing conservation and welfare in ex situ management of the extinct‐in‐the‐wild sihek: sex‐ and age‐specific causes of mortality and contributions to population growth rate

AbstractEx situ threatened species management has both conservation and welfare objectives and these objectives often align, but can diverge. Areas of agreement can present win‐wins for achieving welfare and conservation objectives, while identifying areas of divergence is important to ensure management strategies achieve balance across objectives. We examined welfare and conservation objectives in the ex situ population of Extinct in the Wild sihek (Guam kingfisher, Todiramphus cinnamominus) by quantifying mortality rates, determining sex‐ and age‐specific causes of mortality and identifying associated welfare domains, as well as quantifying sex‐ and age‐specific differences in reproductive value and contributions to variation in population growth rate (λ). Females had significantly higher mortality rates than males, potentially impacting population viability and suggesting females may be more vulnerable to experiencing lower welfare than males. Mitigating causes of female mortality would therefore present a clear win‐win for both welfare and conservation objectives. Both causes of mortality and contributions to variation in λ were found to differ across sex‐ and age‐classes. In particular, nutritional and metabolic diseases tended to impact younger age‐classes and these age‐classes had large contributions to variation in λ. Mitigation of these diseases could therefore also present a win‐win for welfare and conservation objectives. However, we also identified a potential divergence between objectives: a major cause of female mortality was reproductive disease with older aged females primarily affected, but older aged females contributed little to variation in λ and had low reproductive value. Developing mitigation strategies for reproductive disease could therefore aid welfare objectives but have little benefit for conservation objectives, suggesting careful balancing across objectives is required. Our results highlight the need to explicitly consider conservation and welfare objectives in threatened species management, in particular in the context of an increasing conservation need for ex situ population management, coupled with increasing social concern for animal welfare.

Filial Cannibalism Leads to Chronic Nest Failure of Eastern Hellbender Salamanders (Cryptobranchus alleganiensis).

AbstractIn species that provide parental care, parents will sometimes cannibalize their own young (i.e., filial cannibalism). Here, we quantified the frequency of whole-clutch filial cannibalism in a species of giant salamander (eastern hellbender; Cryptobranchus alleganiensis) that has experienced precipitous population declines with unknown causes. We used underwater artificial nesting shelters deployed across a gradient of upstream forest cover to assess the fates of 182 nests at 10 sites over 8 years. We found strong evidence that nest failure rates increased at sites with low riparian forest cover in the upstream catchment. At several sites, reproductive failure was 100%, mainly due to cannibalism by the caring male. The high incidence of filial cannibalism at degraded sites was not explained by evolutionary hypotheses for filial cannibalism based on poor adult body condition or low reproductive value of small clutches. Instead, larger clutches at degraded sites were most vulnerable to cannibalism. We hypothesize that high frequencies of filial cannibalism of large clutches in areas with low forest cover could be related to changes in water chemistry or siltation that influence parental physiology or that reduce the viability of eggs. Importantly, our results identify chronic nest failure as a possible mechanism contributing to population declines and observed geriatric age structure in this imperiled species.

Fitness cost of imidacloprid resistance in the cotton-staining bug, Dysdercus koenigii

Dysdercus koenigii, a serious cotton-staining insect pest in many countries, has shown high resistance to imidacloprid, a systemic neonicotinoid insecticide used to control sap-sucking pests. With the aim of creating an effective management strategy, the biological traits of susceptible (SS) and imidacloprid-resistant (Imida-RS) D. koenigii, as well as their reciprocal crosses (CR1 and CR2), were investigated here using a life table established on age, stage, and two-sex patterns. Compared with SS D. koenigii, Imida-RS and CR1 strains had lower relative fitness (0.80 and 0.47, respectively) and fecundity (eggs per female); prolonged egg duration and a prolonged adult preoviposition period; shorter nymphal duration, male/female total longevity, and oviposition days, and a shorter total preoviposition period. However, there were no differences among strains in nymphal survival rates and female ratio. The CR2 D. koenigii had similar relative fitness value (1.09), suggested no fitness cost in most of the parameters. Demographic parameters, including net reproductive rate, were lower in the Imida-RS strain than in SS and CR2 D. koenigii. Similarly, the Imida-RS and CR1 strains had shorter generation time and doubling time, lower reproductive value and life expectancy relative to the SS and CR2 D. koenigii. In addition, age-specific fecundity was negatively affected in the CR1 strain compared with the other strains. These findings could help facilitate the development of rational D. koenigii control strategies.

Hunting strategies to increase detection of chronic wasting disease in cervids

The successful mitigation of emerging wildlife diseases may involve controversial host culling. For livestock, ‘preemptive host culling’ is an accepted practice involving the removal of herds with known contact to infected populations. When applied to wildlife, this proactive approach comes in conflict with biodiversity conservation goals. Here, we present an alternative approach of ‘proactive hunting surveillance’ with the aim of early disease detection that simultaneously avoids undesirable population decline by targeting demographic groups with (1) a higher likelihood of being infected and (2) a lower reproductive value. We applied this harvesting principle to populations of reindeer to substantiate freedom of chronic wasting disease (CWD) infection. Proactive hunting surveillance reached 99% probability of freedom from infection (<4 reindeer infected) within 3–5 years, in comparison to ~10 years using ordinary harvest surveillance. However, implementation uncertainties linked to social issues appear challenging also with this kind of host culling.

Evolutionary-adaptive and nonadaptive causes of infant attack/desertion in mammals: Toward a systematic classification of child maltreatment.

Behaviors comparable to human child maltreatment are observed widely among mammals, in which parental care is mandatory for offspring survival. This article first reviews the recent findings on the neurobiological mechanisms for nurturing (infant caregiving) behaviors in mammals. Then the major causes of attack/desertion toward infants (conspecific young) in nonhuman mammals are classified into five categories. Three of the categories are 'adaptive' in terms of reproductive fitness: (i) attack/desertion toward non-offspring; (ii) attack/desertion toward biological offspring with low reproductive value; and (iii) attack/desertion toward biological offspring under unfavorable environments. The other two are nonadaptive failures of nurturing motivation, induced by: (iv) caregivers' inexperience; or (v) dysfunction in caregivers' brain mechanisms required for nurturing behavior. The proposed framework covering both adaptive and nonadaptive factors comprehensively classifies the varieties of mammalian infant maltreatment cases and will support the future development of tailored preventive measures for each human case. Also included are remarks that are relevant to interpretation of available animal data to humans: (1) any kind of child abuse/neglect is not justified in modern human societies, even if it is widely observed and regarded as adaptive in nonhuman animals from the viewpoint of evolutionary biology; (2) group-level characteristics cannot be generalized to individuals; and (3) risk factors are neither deterministic nor irreversible.

Flirting with danger: predation risk interacts with male condition to influence sexual display

AbstractSexual signaling coevolves with the sensory systems of intended receivers; however, predators may be unintended receivers of sexual signals. Conspicuous aerial displays in some species may place males at high risk of predation from eavesdropping predators. There are three different hypotheses to explain how signaling males can deal with increased predation risk: (1) males invest in survival by decreasing signal conspicuousness; (2) males invest in reproduction by increasing signal conspicuousness; and (3) male response is condition-dependent according to his residual reproductive value. Here, we used blue-black grassquits (Volatinia jacarina) to test these hypotheses, asking whether males modify leap displays under different levels of predation risk. Grassquit males develop an iridescent nuptial plumage and spend considerable time emitting a multimodal signal: while leaping from a perch, males clap their wings above their heads and emit a high-pitched short song. We exposed males to predator and nonpredator playbacks while video recording their displays. We found interactions between predation risk and 2 male condition variables (ectoparasite infestation and proportion of nuptial plumage coverage) that influenced display behavior. Less parasitized males and those with higher proportion of nuptial plumage showed no change in display behavior, while more parasitized males and those with lower proportion of nuptial plumage increased the vigor of displays under predation risk. In other words, males with low residual reproductive value increased reproductive effort when there was a high risk of extrinsic death. Our study provides some empirical support for the terminal investment hypothesis.

Male Gammarus roeseli provide smaller ejaculates to females infected with vertically transmitted microsporidian parasites

The effects of parasites on the reproduction of their hosts are widespread, but studies investigating the effect of female parasitic status on sperm allocation in males, a form of postcopulatory mate choice, remain scarce. Because males are often sperm limited, strategic sperm investment, in which females of low reproductive value receive fewer sperm, is predicted to occur to maximize long-term male reproductive success. In this study based on pairs collected in natura, we investigated how Gammarus roeseli (Crustacea: Amphipoda) males allocated sperm when paired with females infected with the vertically transmitted, sex ratio-distorting, microsporidian parasites, Nosema granulosis or Dictyocoela sp. Since infected females had similar fecundity to uninfected ones, and offspring of females infected with N. granulosis showed a higher survival rate, we predicted equivalent or even larger sperm investment from males paired with infected females. Contrary to our predictions, males paired with infected females had a lower sperm count before insemination and provided smaller ejaculates than those paired with uninfected females. This pattern suggests either a strategic sperm investment as a function of the female's parasitic status, or that males in good condition had a higher probability of pairing with uninfected females than those in poor condition.

Bacteria Use Collective Behavior to Generate Diverse Combat Strategies

Animals have evolved a wide diversity of aggressive behavior often based upon the careful monitoring ofother individuals. Bacteria are also capable of aggression, with many species using toxins to kill or inhibit their competitors. Like animals, bacteria also have systems to monitor others during antagonistic encounters, but how this translates into behavior remains poorly understood. Here, we use colonies of Escherichia coli carrying colicin-encoding plasmids as a model for studying antagonistic behavior. We show that in the absence of threat, dispersed cells with low reproductive value produce colicin toxins spontaneously, generating efficient pre-emptive attacks. Cells can also respond conditionally to toxins released by clonemates via autoinduction orother genotypes via competition sensing. The strength of both pre-emptive and responsive attacks varies widely between strains. We demonstrate that this variability occurs easily through mutation by rationally engineering strains to recapitulate the diversity in naturally occurring strategies. Finally, we discover that strains that can detect both competitors and clonemates are capable of massive coordinated attacks on competing colonies. This collective behavior protects established colonies from competitors, mirroring the evolution of alarm calling in the animal world.

Parasite dispersal risk tolerance is mediated by its reproductive value

Parasite dispersal theory draws heavily upon epidemiological SIR models in which host status (susceptible (S), infected (I), or recovered (R)) is used to study parasite dispersal evolution. In contrast to these extrinsically host-centric drivers, in this study we focus on an intrinsic driver, the parasite's reproductive value (predicted future offspring) as a regulator of the extent to which the individual will engage in risky dispersal behaviour. As a model system we use the honeybee Apis mellifera and its ectoparasite, the mite Varroa destructor. Mite reproduction happens exclusively inside cells of bee brood, and newly emerged fecund mites may parasitize either a homocolonial brood cell (low risk dispersal) or emigrate to a new bee colony via phoretic attachment to mature forager bees (high risk dispersal). In an empirical bioassay, prepartum mites (high reproductive value) and postpartum mites (low reproductive value) were offered a choice of newly emerged homocolonial worker bees (low risk), homocolonial pollen forager bees (high risk), or heterocolonial pollen foragers (high risk). A preference for newly emerged bees was earlier and more strongly sustained among prepartum mites. This suggests comparatively greater dispersal risk tolerance among postpartum mites with lower reproductive value. A dangerous bid for dispersal may be adaptive if the individual has already successfully reproduced and the rewards for successful dispersal are sufficiently large.

Silk wrapping of nuptial gifts aids cheating behaviour in male spiders

Sexual traits, such as nuptial gifts, are costly and often condition-dependent. Males should be under selection to reduce these costs without impairing their reproductive success. Spider gifts consist of silk-wrapped food, but may also consist of worthless (non-nutritive) donations that successfully lead to mating, despite yielding shorter copulations. Worthless gifts may either represent a cheaper cheating strategy or the inability to produce genuine gifts due to resource limitations (i.e. poor body condition). Unless energetic constraints limit expenditure in silk, males should apply more silk to worthless gifts to compensate for their lower reproductive value. We ask whether in Pisaura mirabilis 1) worthless gifts are condition-dependent and 2) males strategically use silk based on gift type (genuine vs worthless). We tested whether male body condition explains the gift-giving strategy and compared silk amounts covering each gift type, in gifts collected from the field and produced in the laboratory by males given different feeding regimes. Our findings show that worthless gifts are not promoted by poor body condition or limited resources. They rather result from a cheating strategy evolved to opportunistically reduce the costs of genuine gifts while ensuring nutritional advantages, with cheaters gaining body mass. Males applied more silk to worthless gifts regardless of their body condition or feeding state, suggesting they can strategically adjust silk expenditure despite its costs. By masking gift contents and prolonging female feeding, silk is crucial for the maintenance of cheating, likely resulting from an evolutionary arms race between male deception and female assessment.

Water mold infection but not paternity induces selective filial cannibalism in a goby.

Many animals heavily invest in parental care but still reject at least some of their offspring. Although seemingly paradoxical, selection can favor parents to neglect offspring of particularly low reproductive value, for example, because of small survival chances. We here assess whether filial cannibalism (FC), where parents routinely eat some of their own young, is selective in response to individual offspring reproductive value. We performed two independent laboratory experiments in the common goby (Pomatoschistus microps) to test whether caring fathers preferentially cannibalize eggs of a given infection history and paternity. While males did not discriminate kin from nonkin eggs, they consumed significantly more eggs previously exposed to water mold compared to uninfected eggs. Our findings clearly show that parents differentiate between eggs based on differences in egg condition, and thus complement the prevailing view that FC arises for energetic reasons. By preventing the spread of microbial infections, the removal of molded eggs can constitute an important component of parental care and may represent a key driver of selective FC in a wide array of parental fish.

Contribution of released captive-bred Mallards to the dynamics of the natural population

The consequences of releasing captive-bred game animals into the wild have received little attention, despite their potential demographic impact, as well as costs and/or benefits for recipient populations. If restocking aims at increasing harvest opportunities, increased hunting pressure is expected, which would then be supported by either wild or released individuals. On the other hand, the wild recipient population may benefit from the release of captive-bred conspecifics if this reduces hunting pressure on the former through dilution of risk or selective harvesting of captive-bred individuals. Here, we modelled a Mallard (Anas platyrhynchos) population consisting of wild individuals supplemented by captive-bred conspecifics, a very common practice in Europe over the last 40 years. The objective was to test the effect of an increase of harvest rate on released and wild individuals, respectively. Our results show that, due to the low reproductive value of the released Mal-lards, the population was hardly affected by a change in harvest of these low performance individuals. Conversely, a 15 percent increase in harvest rate of the wild individuals would lead to a quick decline of the population. We discuss these results in the context of the Camargue population, located in the South of France, which has experienced an increase in Mallard harvest without apparent reduction of population size. We suggest that this has only been possible due to the release of captive-bred Mallards.

Control of parental investment changes plastically over time with residual reproductive value.

Evolutionary conflict between parents and offspring over parental resource investment is a significant selective force on the traits of both parents and offspring. Empirical studies have shown that for some species, the amount of parental investment is controlled by the parents, whereas in other species, it is controlled by the offspring. The main difference between these two strategies is the residual reproductive value of the parents or opportunities for future reproduction. Therefore, this could explain the patterns of control of parental investment at the species level. However, the residual reproductive value of the parents will change during their lifetime; therefore, parental influence on the amount of investment can be expected to change plastically. Here, we investigated control of parental investment when parents were young and had a high residual reproductive value, compared to when they were old and had a low residual reproductive value using a cross-fostering experiment in the burying beetle Nicrophorus quadripunctatus. We found that parents exert greater control over parental investment when they are young, but parental control is weakened as the parents age. Our results demonstrate that control of parental investment is not fixed, but changes plastically during the parent's lifetime.

Reefscapes of fear: predation risk and reef hetero‐geneity interact to shape herbivore foraging behaviour

Predators can exert strong direct and indirect effects on ecological communities by intimidating their prey. The nature of predation risk effects is often context dependent, but in some ecosystems these contingencies are often overlooked. Risk effects are often not uniform across landscapes or among species. Indeed, they can vary widely across gradients of habitat complexity and with different prey escape tactics. These context dependencies may be especially important for ecosystems such as coral reefs that vary widely in habitat complexity and have species-rich predator and prey communities. With field experiments using predator decoys of the black grouper (Mycteroperca bonaci), we investigated how reef complexity interacts with predation risk to affect the foraging behaviour and herbivory rates of large herbivorous fishes (e.g. parrotfishes and surgeonfishes) across four coral reefs in the Florida Keys (USA). In both high and low complexity areas of the reef, we measured how herbivory changed with increasing distance from the predator decoy to examine how herbivorous fishes reconcile the conflicting demands of avoiding predation vs. foraging within a reefscape context. We show that with increasing risk, herbivorous fishes consumed dramatically less food (ca. 90%) but fed at a faster rate when they did feed (ca. 26%). Furthermore, we show that fishes foraging closest to the predator decoy were 40% smaller than those that foraged at further distances. Thus, smaller individuals showed muted response to predation risk compared to their larger counterparts, potentially due to their decreased risk to predation or lower reproductive value (i.e. the asset protection principle). Habitat heterogeneity mediated risk effects differently for different species of herbivores, with predation risk more strongly suppressing herbivore feeding in more complex areas and for individuals at higher risk of predation. Predators appear to create a reefscape of fear that changes the size structure of herbivores towards smaller individuals, increases individual feeding rates, but suppresses overall amounts of primary producers consumed, potentially altering patterns of herbivory, an ecosystem process critical for healthy coral reefs.

Mating rock shrimp hedge their bets: old males take greater risk, but only after careful assessment of the investment scenario

Mature organisms often have to trade reproductive opportunities against the need to survive, especially in species with exaggerated, sexually selected traits. Life history theory predicts that old males with low residual reproductive value (RRV) would accept greater risk for current reproduction than their younger counterparts. Accordingly, we tested the prediction that, under predation risk, old males of the rock shrimp Rhynchocinetes typus pair with females faster and for a longer time than young males do. We exposed young and old dominant males (in the final ontogenetic stage, called “robustus”) to a female in the absence and presence of a predator. As predicted, older robustus males modified their mating behavior when exposed to a predator. However, in contrast to the prediction, they delayed female seizure under predation risk, possibly to carefully assess the actual threat before initiating female guarding. Once they had established the mate-guarding position, old robustus males did not interrupt it until the end of female spawning and, in the presence of predators, even guarded the female significantly longer than in predator-free treatments. In contrast, younger robustus males did not delay female seizure but abandoned the female repeatedly when a predator was present, suggesting that they perceived and responded to the predation risk. Our results suggest that older robustus males have the experience to assess threats before engaging in risky behaviors that bolster their reproductive success. Although consistent with the theory that low RRV individuals should accept greater reproductive risk, we suggest that old individuals do not recklessly engage in risky behaviors but rather cautiously evaluate the threats before investing in a potentially terminal reproductive event.

Inclusive fitness effects can select for cancer suppression into old age

Natural selection can favour health at youth or middle age (high reproductive value) over health at old age (low reproductive value). This means, all else being equal, selection for cancer suppression should dramatically drop after reproductive age. However, in species with significant parental investment, the capacity to enhance inclusive fitness may increase the reproductive value of older individuals or even those past reproductive age. Variation in parental investment levels could therefore contribute to variation in cancer susceptibility across species. In this article, we describe a simple model and framework for the evolution of cancer suppression with varying levels of parental investment and use this model to make testable predictions about variation in cancer suppression across species. This model can be extended to show that selection for cancer suppression is stronger in species with cooperative breeding systems and intergenerational transfers. We consider three cases that can select for cancer suppression into old age: (i) extended parental care that increases the survivorship of their offspring, (ii) grandparents contributing to higher fecundity of their children and (iii) cooperative breeding where helpers forgo reproduction or even survivorship to assist parents in having higher fecundity.

Age affects escape behavior by the zebra-tailed lizard (Callisaurus draconoides) more strongly than in other lizards

Prey of different ages may exhibit differences in escape behavior, including flight initiation distance (FID – predator-prey distance when escape begins) and distance fled before stopping (DF). Escape theory predicts FID and, in some circumstance, DF, based on trade-offs between conflicting cost of not fleeing (predation risk) and cost of fleeing (primarily opportunities to enhance fitness lost by fleeing). The prey’s expected lifetime fitness when an encounter begins also affects escape decisions. Because hatchling and adult lizards may differ in ways that affect all three of these factors, a priori prediction of age differences is not possible without measurements of all three. In a field study I found that hatchling zebra-tailed lizards (Callisaurs draconoides) had much shorter FID and DF than adults. These relationships were not affected by distance to refuge, which did not differ between ages, and refuge use was infrequent. The findings agree with those of all but one previous study of age differences, suggesting that hatchling lizards typically have shorter FID and DF than adults because they 1) assess risk as being lower due to lower attractiveness to or detectability by predators, lack of experience or greater maneuverability, 2) have greater opportunity cost due to the need for rapid growth and good body condition before winter, and possibly 3) have lower residual reproductive value due to higher mortality rate than adults. Effects of age and size are confounded, and smaller size may be the major reason for the shorter FID and distance fled of hatchlings.

Age and sex-selective predation moderate the overall impact of predators.

Currently, there is no general agreement about the extent to which predators impact prey population dynamics and it is often poorly predicted by predation rates and species abundances. This could, in part be caused by variation in the type of selective predation occurring. Notably, if predation is selective on categories of individuals that contribute little to future generations, it may moderate the impact of predation on prey population dynamics. However, despite its prevalence, selective predation has seldom been studied in this context. Using recoveries of ringed tawny owls (Strix aluco) predated by 'superpredators', northern goshawks (Accipiter gentilis) as they colonized the area, we investigated the extent to which predation was sex and age-selective. Predation of juvenile owls was disproportionately high. Amongst adults, predation was strongly biased towards females and predation risk appeared to increase with age. This implies age-selective predation may shape the decline in survival with age, observed in tawny owls. To determine whether selective predation can modulate the overall impact of predation, age-based population matrix models were used to simulate the impact of five different patterns of age-selective predation, including the pattern actually observed in the study site. The overall impact on owl population size varied by up to 50%, depending on the pattern of selective predation. The simulation of the observed pattern of predation had a relatively small impact on population size, close to the least harmful scenario, predation on juveniles only. The actual changes in owl population size and structure observed during goshawk colonization were also analysed. Owl population size and immigration were unrelated to goshawk abundance. However, goshawk abundance appeared to interact with owl food availability to have a delayed effect on recruitment into the population. This study provides strong evidence to suggest that predation of other predators is both age and sex-selective and that selective predation of individuals with a low reproductive value may mitigate the overall impact of predators on prey population dynamics. Consequently, our results highlight how accounting for the type of selective predation occurring is likely to improve future predictions of the overall impact of predation.

Changing reproductive effort within a semelparous reproductive episode.

• Life-history theory predicts a trade-off between current and future reproduction for iteroparous organisms-as individuals age, the expected value of future reproduction declines, and thus reproductive effort is expected to be higher in later clutches than in earlier. In contrast, models explaining the evolution of semelparity treat semelparous reproduction as instantaneous, with no scope for intraindividual variation. However, semelparous reproduction is also extended, but over shorter time scales; whether there are similar age- or stage-specific changes in reproductive effort within a semelparous episode is unclear. In this study, we assessed whether semelparous individuals increase reproductive effort as residual reproductive value declines by comparing the reproductive phenotype of flowers at five different floral positions along a main inflorescence.• Using the herbaceous monocarp Lobelia inflata, we conducted a longitudinal study of 409 individuals including both laboratory and field populations over three seasons. We recorded six reproductive traits-including the length of three phenological intervals as well as fruit size, seed size, and seed number-for all plants across floral positions produced throughout the reproductive episode.• We found that while the rate of flower initiation did not change, flowers at distal (late) floral positions developed more quickly and contained larger seed than flowers at basal (early) floral positions did.• Our results were consistent with the hypothesis that, like iteroparous organisms, L. inflata increases reproductive effort in response to low residual reproductive value.

Pheromone Blend Does not Explain Old Male Mating Advantage in a Butterfly

In several insect species, male mating success is higher in older than in younger males, although condition diminishes dramatically with age. Two hypotheses are under debate to explain the counterintuitive pattern of old male mating advantage: first, an increased eagerness of older males to mate, driven by their low residual reproductive value, and second female preference for older males based on chemical cues such as sex pheromones (female choice hypothesis). In a series of experiments, we manipulated female olfaction, male pheromone blend and female age to test whether old male mating advantage prevails when the influence of male sex pheromones is controlled for, using the tropical butterfly Bicyclus anynana as model. We found that older males had a higher mating success than younger ones irrespective of female scent-sensitivity and irrespective of male pheromone blend. Interestingly, older males were found to court more often and for longer time bouts than younger males. These results were independent of female age, although younger males courted younger females more often and for longer bouts than older females. Taken together, our results indicate that male courtship activity (1) is higher in older compared to younger males and (2) increases the mating success of older males. Olfaction and sensing pheromones, in contrast, were not a necessary prerequisite for old male mating advantage to occur and may use other cues than pheromones to assess male quality.