Roaring Behavior of Two Syntopic Howler Species (Alouatta caraya and A. guariba clamitans): Evidence Supports the Mate Defense Hypothesis

Long-distance calls are loud vocalizations involved in within and between group communication in animals. These calls may maintain cohesion with group members or communicate the ownership of valuable resources such as territory, food, or mates to individuals from other groups. In howlers (Alouatta spp.), three nonmutually exclusive hypotheses suggest that the ultimate function of roaring (howling) behavior is to protect resources from neighboring groups. The space/food defense hypothesis maintains that roars are used to gain exclusive access to food; the mate defense hypothesis holds that roars ensure exclusive access to mates; and the infanticide avoidance hypothesis states that the roaring behavior serves to avoid male takeovers and infanticide. To test these three hypotheses, we conducted a study on black-and-gold howlers (Alouatta caraya) and brown howlers (A. guariba clamitans) living in syntopy at El Pi?alito provincial park in northeast Argentina. We recorded 12 mo of data on the roaring behavior of two groups of each species, along with data on food availability and diet. Although all four groups overlapped extensively in their use of food resources during the study period, roars occurred much more frequently during interactions between groups of the same species than between groups of different species. Roaring frequency was not higher during the lean season, when high-quality food was less abundant. Howlers did not roar more frequently at home range boundaries, nor were roaring bouts spatially associated with valuable feeding resources. Males participated in all of the roaring bouts, whereas females participated in only 29% of them. Adults did not roar more frequently when there were unweaned infants in the group, as expected if roaring behavior decreases infanticide risk. These results provide no support for the food defense or infanticide avoidance hypotheses, but support predictions derived from the mate defense hypothesis.     

Infanticide and control of reproduction in cooperative and communal breeders

Many communal breeders are characterized by a conflict over who gets to reproduce, with dominant individuals often claiming the largest share of reproduction in the group. How do dominants control breeding in these species? Although infanticide has often been invoked as a means of control, previous theoretical work on indiscriminate killing of young did not support this idea. There is, however, increasing evidence from field studies in both vertebrates and insects that infanticidal individuals can discriminate between their own offspring and those of other group members, and thus avoid the risk of accidentally killing their own progeny. In a simple game-theoretical model we demonstrate that the capacity for discriminate infanticide can promote high reproductive skew even though few or no offspring are actually killed. When discrimination is good and offspring are cheap to produce, the threat of infanticide prevents the subordinate cobreeder from adding many young to the joint brood, and no killing need occur. High levels of infanticide tend to occur only when discrimination is poor, costs of offspring production are low and/or relatedness is low.     

Infanticide and effectiveness of pup protection in bank voles: does the mother recognise a killer?

Infanticide, the killing of conspecific young, has been documented in numerous species of mammals, especially rodents. In that infanticide is costly to the victim mother, natural selection should favour counter-strategies by females to protect their pups. We studied the frequency of infanticide by male and female bank voles (Clethrionomys glareolus) and the effectiveness of dams in recognising and deterring infanticide. In trials in which unprotected pups were exposed to voles of both sexes, one third of male and female intruders killed pups. When mothers were present at the nest site, not a single female and only 2 of 25 males were able to commit infanticide. Females acted aggressively towards all intruders and hence did not discern between infanticidal and non-infanticidal males and females. Aggression of dams against any intruder indicates that all strange individuals near the nest site of a territorial species form an equal threat to pups. However, the presence of the aggressive dam is sufficient to deter most intruders from harming offspring by keeping them at a distance from the nest site. Heat run before mating, in a species with postpartum oestrus and vulnerable pups in the nest, also might lure potential infanticidal males away from the nest site and obscure the nest location. Received in revised form: 17 October 2001 Electronic Publication     

Adaptive switch from infanticide to parental care: how do beetles time their behaviour?

Abstract In species where parents may commit infanticide, temporal kin recognition can help ensure parents kill unrelated young but care for their own offspring. This is not true recognition, but rather depends on accurate timing of the arrival of young and a behavioural switch from killing to caring for offspring. Mistakes have clear fitness consequences; how do species that use temporal kin recognition ensure accurate timing? We manipulated photic cues and show that the switch from infanticide to parental care in the burying beetle Nicrophorus vespilloides depends on day‐length inputs. Extending the light period after carcass discovery influenced timing of both oviposition and the cessation of infanticide. Manipulation of the light : dark cycle after oviposition also influenced timing of the switch to parental care. The timing mechanism is therefore sensitive to photic cues and access to a carcass and is not triggered by oviposition. The behavioural switch is directly related to the timing mechanism rather than changes in reproductive physiology. Given the conserved nature and extensive homology of genetic influences on biological timing, we speculate that the molecular mechanisms regulating circadian behaviour may have been co‐opted to allow beetles to determine how much time has passed after carcass discovery even though this is over 50 h.     

Is Mating Alone Enough to Inhibit Infanticide in Male Bank Voles?

Infanticide, the killing of conspecific young, is commonly recognized as an adaptive behavioural strategy enhancing the fitness of the perpetrator. Infanticide is supposed to be inhibited in several male rodent species after mating with a time lag to the time when perpetrators own offspring would be born. This is because males with no parental care do not recognize their own offspring. It has been suggested that copulation alone is enough to inhibit infanticidal behaviour in male rodents. Infanticidal behaviour occurs in more than 50% of male bank voles (Myodes glareolus), and offspring loss because of infanticide may have a great effect on breeding success and population recruitment. In a laboratory experiment, we studied whether infanticidal male bank voles after successful mating stop the killing of pups. Infanticidal males were paired with a female until successful copulation. After the young were born, the males’ infanticidal behaviour was studied from the time of expected birth of own pups until their post‐weaning age. We predicted that mated infanticidal males are inhibited from committing infanticide especially during the time period when pups are less than 10 d old. Against our prediction, 67% of the infanticidal males continued the killing of pups in the age of 3 d. Infanticidal behaviour remained stable, and half of the males were infanticidal still at the age of weaning of pups. Our results are contradictory to previous studies, as we observed no inhibition of infanticide during early life of pups nor increase in infanticide again when their own offspring would have reached the ‘safe’ age and size after weaning. We suggest that mating alone is not sufficient to inhibit infanticide. Thus, we suggest that other cues of the female with whom the male mated with or on her territory are needed for inhibition to occur.     

Sexually selected infanticide in a polygynous bat

Background

Adult individuals of many species kill unrelated conspecific infants for several adaptive reasons ranging from predation or resource competition to the prevention of misdirected parental care. Moreover, infanticide can increase the reproductive success of the aggressor by killing the offspring of competitors and thereafter mating with the victimized females. This sexually selected infanticide predominantly occurs in polygynous species, with convincing evidence for primates, carnivores, equids, and rodents. Evidence for bats was predicted but lacking.

Methodology/Principal Findings

Here we report the first case, to our knowledge, of sexually selected infanticide in a bat, the polygynous white-throated round-eared bat, Lophostoma silvicolum. Behavioral studies in a free-living population revealed that an adult male repeatedly attacked and injured the pups of two females belonging to his harem, ultimately causing the death of one pup. The infanticidal male subsequently mated with the mother of the victimized pup and this copulation occurred earlier than any other in his harem.

Conclusions/Significance

Our findings indicate that sexually selected infanticide is more widespread than previously thought, adding bats as a new taxon performing this strategy. Future work on other bats, especially polygynous species in the tropics, has great potential to investigate the selective pressures influencing the evolution of sexually selected infanticide and to study how infanticide impacts reproductive strategies and social structures of different species.     

Two in one: cryptic species discovered in biological control agent populations using molecular data and crossbreeding experiments

There are many examples of cryptic species that have been identified through DNA‐barcoding or other genetic techniques. There are, however, very few confirmations of cryptic species being reproductively isolated. This study presents one of the few cases of cryptic species that has been confirmed to be reproductively isolated and therefore true species according to the biological species concept. The cryptic species are of special interest because they were discovered within biological control agent populations. Two geographically isolated populations of Eccritotarsus catarinensis (Carvalho) [Hemiptera: Miridae], a biological control agent for the invasive aquatic macrophyte, water hyacinth, Eichhornia crassipes (Mart.) Solms [Pontederiaceae], in South Africa, were sampled from the native range of the species in South America. Morphological characteristics indicated that both populations were the same species according to the current taxonomy, but subsequent DNA analysis and breeding experiments revealed that the two populations are reproductively isolated. Crossbreeding experiments resulted in very few hybrid offspring when individuals were forced to interbreed with individuals of the other population, and no hybrid offspring were recorded when a choice of mate from either population was offered. The data indicate that the two populations are cryptic species that are reproductively incompatible. Subtle but reliable diagnostic characteristics were then identified to distinguish between the two species which would have been considered intraspecific variation without the data from the genetics and interbreeding experiments. These findings suggest that all consignments of biological control agents from allopatric populations should be screened for cryptic species using genetic techniques and that the importation of multiple consignments of the same species for biological control should be conducted with caution.     

Exposure to a novel male during late pregnancy influences subsequent growth of offspring during lactation

In mammals, allocation to reproduction can either be primed or suppressed in relation to cues from other individuals. Some conspecifics (e.g. potential mates) may enhance an individual's ability to reproduce but others may have a detrimental effect on reproductive success. One widely studied response to conspecific cues, the ‘Bruce effect’, occurs when pregnant females abort their pregnancies after exposure to a novel male. It has been suggested that this response has evolved as a counter‐tactic to the threat of infanticide posed by novel males. In some species, like mice, pregnancy termination will only occur if females are exposed to the unfamiliar male during a brief critical period early in pregnancy, which is surprising considering that an unfamiliar male threatens infanticide whenever present, and in particular near to birth. We demonstrate that female mice experiencing novel males during late pregnancy also alter their investment in progeny, but in a more subtle manner than previously observed. Females exposed to an unfamiliar male during late pregnancy give birth to offspring of a comparable weight to those produced by females exposed to the paternal male, but these offspring grow more slowly over lactation. As a consequence, offspring from these females weigh less at weaning. Modification of their growth trajectory, however, allows these offspring to catch up to normal weights by adulthood. Thus, cues of unfamiliar males, and possibly their associated threat of infanticide, can produce more wide‐ranging effects on maternal investment than previously recognized.     

Strategies and counterstrategies to infanticide in mammals

I analyse and summarize the empirical evidence in mammals supporting alternative benefits that individuals may accrue when committing nonparental infanticide. Nonparental infanticide may provide the perpetrator with nutritional benefits, increased access to limited resources, increased reproductive opportunities, or it may prevent misdirecting parental care to unrelated offspring. The possibility that infanticide is either a neutral or maladaptive behaviour also is considered. I devote the second half of this article to reviewing potential mechanisms that individuals may use to prevent infanticide. These counterstrategies include the early termination of pregnancy, direct aggression by the mother against intruders, the formation of coalitions for group defence, the avoidance of infanticidal conspecifics, female promiscuity, and territoriality. I evaluate the support for each benefit and counterstrategy across different groups of mammals and make suggestions for future research.     

WHY MOTHERS DO NOT RESIST INFANTICIDE: A COST-BENEFIT GENETIC MODEL

Infanticide has recently been observed in several primate species while female counterstrategies are seemingly rare. The question of why mothers do not increase their resistance to infanticide is investigated using a haploid two-locus model. A hypothesis that mothers can recover lost offspring by gaining more grandchildren is rejected in most cases, and it is shown that costs and benefits for both males and females have the strongest influence on the evolution of infanticide and obedience to it. An estimation of parameters for a natural population of hanuman langurs suggests that infanticide is more advantageous than noninfanticide and the costs of resistance, compared to obedience, is higher than its benefits. Data from other studies on primate infanticide are discussed in the light of results of the model.     

Infanticide and Maternal Offspring Defence in European Rabbits under Natural Breeding Conditions

Infanticide is an important source of mortality of dependent offspring in several mammal species, whereas female conspecifics are often the perpetrators. This has led to maternal counter‐strategies, such as the defence of the nests. However, cases of infanticide are hard to detect in the field, and studies on maternal offspring defence behaviour under natural breeding conditions are scarce. We conducted such a study on the European rabbit (Oryctolagus cuniculus), which is usually considered to show low maternal care. The study was carried out over 5 yr on a field enclosure population. We (1) studied infanticide rates and the impact of potential determinants: the group density and age structure of the females’ rank hierarchy within the groups; we used the latter as an estimator of social group stability. We (2) studied if mothers defend their breeding burrow against approaching, potentially infanticidal females. Overall, we recorded infanticide in 5% of all litters; infanticide was the cause in 12% of cases of litter mortality. The proportion of infanticide was 7% higher in groups where same‐age females occupied successive rank positions than in groups where the females’ rank hierarchy had a more heterogeneous and linear age structure. We hypothesize that social instability in the former groups was the reason for the increased infanticide risk. Infanticide rates were not correlated with group density and did not differ among mothers with different social ranks. Infanticide occurred exclusively during the first 10 d after parturition. During this time, mothers stayed closer to their breeding burrows than shortly before parturition or during later lactation. Moreover, mothers were more aggressive against other females in proximity to their breeding burrow than in more distant areas. We suggest that the pattern of spacing behaviour and intrasexual aggression of rabbit mothers are an adaptive response to the occurrence of female infanticidal behaviour.     

A case of infanticide in the Spot-billed Duck in circumstances of high breeding density

The first observations of infanticide by a precocial avian species, Spot-billed Duck (Anas poecilorhyncha), were recorded on a small pond at Yatsu tidal flat, central Japan, from May to June 2000, where six families of conspecific and one Gadwall A. strepera family, respectively, occupied territories. A female Spot-billed Duck with 11 ducklings attacked ducklings of all the other families killing eight conspecifics and three of the Gadwall. High breeding density (15.0 families/ha) may have increased the aggression of the female. Electronic Publication     

Two cases of mother–infant cannibalism in orangutans

Observations of ape cannibalism have to this point been limited to chimpanzees (Pan troglodytes) where it is associated with infanticide and consumption by unrelated individuals (Watts and Mitani, Primates 41(4):357–365, 2000). Here we report for the first time observations of two unrelated female Sumatran orangutans (Pongo abelii) cannibalizing the remains of their infants on different occasion, a behavior never before reported in any ape species. The two orangutans were wild-born rehabilitated individuals, and had been reintroduced to an area hosting a largely unregulated primate tourism industry and experienced restricted ranging conditions. Though it is possible that this is a strategy to regain energy and nutrients or a result of individual history, comparative data suggest that this is an aberrant behavior which may be linked to environmental stressors within the area. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Polyandry enhances offspring survival in an infanticidal species

The adaptive significance of polyandry is an intensely debated subject in sexual selection. For species with male infanticidal behaviour, it has been hypothesized that polyandry evolved as female counterstrategy to offspring loss: by mating with multiple males, females may conceal paternity and so prevent males from killing putative offspring. Here we present, to our knowledge, the first empirical test of this hypothesis in a combined laboratory and field study, and show that multiple mating seems to reduce the risk of infanticide in female bank voles Myodes glareolus. Our findings thus indicate that females of species with non-resource based mating systems, in which males provide nothing but sperm, but commit infanticide, can gain non-genetic fitness benefits from polyandry.     

Variance in the reproductive success of dominant male mountain gorillas

Using 30 years of demographic data from 15 groups, this study estimates how harem size, female fertility, and offspring survival may contribute to variance in the siring rates of dominant male mountain gorillas throughout the Virunga Volcano Region. As predicted for polygynous species, differences in harem size were the greatest source of variance in the siring rate, whereas differences in female fertility and offspring survival were relatively minor. Harem size was positively correlated with offspring survival, even after removing all known and suspected cases of infanticide, so the correlation does not seem to reflect differences in the ability of males to protect their offspring. Harem size was not significantly correlated with female fertility, which is consistent with the hypothesis that mountain gorillas have minimal feeding competition. Harem size, offspring survival, and siring rates were not significantly correlated with the proportion of dominant tenures that occurred in multimale groups versus one-male groups; even though infanticide is less likely when those tenures end in multimale groups than one-male groups. In contrast with the relatively small contribution of offspring survival to variance in the siring rates of this study, offspring survival is a major source of variance in the male reproductive success of western gorillas, which have greater predation risks and significantly higher rates of infanticide. If differences in offspring protection are less important among male mountain gorillas than western gorillas, then the relative importance of other factors may be greater for mountain gorillas. Thus, our study illustrates how variance in male reproductive success and its components can differ between closely related species.     

Communal Nesting in Asocial Abert's Squirrels: the Role of Social Thermoregulation and Breeding Strategy

The social thermoregulation hypothesis states that endothermic species will communally nest to reduce energy expenditures on thermoregulation. The hypothesis predicts that the frequency of communal nesting should increase with decreasing ambient temperature. The potential costs of communal nesting (e.g., increased predation risk, resource competition, cuckoldry, parasite/disease transmission, or infanticide) could decrease the frequency of communal nesting especially for asocial breeding females with dependent offspring. We examined the effects of ambient temperature and seasonal reproductive activities on the probability of communal nesting in Abert's squirrels (Sciurus aberti) in the Pinaleño Mountains, Arizona. Most squirrels nested consistently with the same partner in mixed‐sex pairs. The proportion of individuals engaging in communal nesting increased with decreasing ambient temperature as predicted by the social thermoregulation hypothesis. The onset of the breeding season greatly reduced the proportion of individuals communally nesting. The negative relationship between ambient temperature and communal nesting supports the use of communal nesting in Abert's squirrels as a mechanism to reduce thermoregulatory costs during cold conditions. The abrupt drop in the frequency of communal nesting during the breeding season is likely due to female abandonment of this behavior. By avoiding communally nesting during the breeding season, females may prevent males from mating with them outside of mating chases, reduce resource competition, and protect offspring from infanticide, diseases, and parasites. Males may gain additional fitness benefits from nesting with females because familiarity with females increases dominance rank in mating activities.     

Infant loss during and after male replacement in gibbons

According to the sexual selection hypothesis, infanticide during resident male replacement is an adaptive strategy that has evolved because the killing of unweaned offspring sired by previous males shortens the inter‐birth intervals of the mothers whose infants are targeted and thereby increases the reproductive fitness of the perpetrator. To test this hypothesis, we describe previously unreported cases of primary male replacement for two gibbon species (Hylobates lar and Nomascus nasutus), and review all other reported cases of primary male replacement in gibbons. Overall, infants were present in nearly half of all cases (16/33, 48%) and of the 18 infants present during replacement, 50% (N = 9) disappeared within 2 months of the event. In four of the five cases where there was sufficient demographic information to identify the likely sire of the subsequent offspring of females that lost infants, the new male was believed to be the sire. Infants were also less likely to die or disappear if the new male and original resident male were possible kin. However, there was no significant difference in the age of infants between those that died or disappeared following replacement and those that survived to weaning (p = .630). Our review of takeover‐related infant loss in gibbons confirms that periods of male instability are risky for unweaned infants and that replacing males benefit from infant loss. Nevertheless, variability in the context of infant loss and difficulties related to data collection in the field make it difficult to test competing hypotheses concerning the mechanisms and functions of infanticide in the small apes.     

Potentially infanticidal behavior in the Amazon river dolphin (<Emphasis Type="Italic">Inia geoffrensis</Emphasis>)

Infanticide by males is a phenomenon common in species in which the reproductive output of large numbers of females can be monopolized by a small number of males. It is thought to increase a male’s fitness, at the expense of the fitness of the infant’s parents, by bringing females into season more quickly. Infanticide by males has been recorded in just three cetacean species. We report aggressive behavior suggestive of infanticide in a fourth, the Amazon river dolphin (Inia geoffrensis). We observed and photographed a series of attacks on a neonate Amazon river dolphin by a large male, with apparent protective behavior by the mother. Although infanticide was not confirmed, the forceful, aggressive behaviors were highly suggestive of infanticidal behavior and represent another important data point for comparative studies of infanticide in mammals. Amazon river dolphins may have a polygynous, polyandrous, or promiscuous mating system, the latter two of which are not the norm in species in which the reproductive output of large numbers of females are monopolized by a small number of males. However, sexual dimorphism, high rates of aggression by males, socio-sexual object-carrying displays by males, and a long interbirth interval suggest that successful male Amazon river dolphins may be able to monopolize a large proportion of mating opportunities, and it is plausible that male dolphins can improve their reproductive success by bringing females into estrous sooner by killing the offspring of other males.     

Not berry hungry? Discovering the hidden food sources of a small fruit specialist,Drosophila suzukii

1. Although polyphagy is widespread among Drosophila, some specialist species have evolved in response to resource competition and other selection factors favouring niche separation. The small fruit specialist Drosophila suzukii Matsumura has evolved a unique serrated ovipositor that allows it to access ripening fruit, a niche unavailable to most Drosophila. However, it is unclear whether ancestral traits (the use of non‐fruit resources) are maintained in this specialist species. 2. In this study, maternal preferences and offspring fitness in response to novel apple, mushroom, and bird manure‐based diets were investigated by comparing oviposition and offspring survival and development on various diets. The effect of those diets on survival at cool temperatures and the effect of natal environment/previous exposure on adult preferences were evaluated. 3. Female D. suzukii accepted non‐fruit diets such as mushroom and bird manure, and offspring completed their larval development on all diets tested. However, D. suzukii did not perform well on diets that included bird manure. By contrast, combinational apple/mushroom diets were associated with greater oviposition, lower mortality, faster development, and larger offspring than other diets. These diets were also associated with increased resistance to cold stress, and preference for these diets was positively affected by previous feeding experience. 4. These data suggest that D. suzukii may use non‐fruit resources when preferred resources are scarce. Given that this pest is adapted to temperate climates, alternative resources might provide seasonal nutritional support when fruit resources are not temporally available, although field data are needed to support this hypothesis.