Population biology of swift (Apus apus) ectoparasites in relation to host reproductive success

Abstract.

• 1 We censused ectoparasite populations of adult and nestling swifts over the course of the host's breeding season. Nearly all of the birds were infested with chewing lice and two-thirds of the nests were infested with louse flies. Feather mites were observed but not quantified.
• 2 Lice and louse flies both showed aggregated distributions among hosts. Louse eggs, hatched lice and adult louse flies had negative binomial distributions, whereas the aggregated distribution of louse fly pupae was not adequately described by negative binomial or Poisson models.
• 3 Transmission of lice from parents to offspring was documented. A comparison of the age structure of lice on parents and offspring indicated that most transmission was by nymphal lice.
• 4 Host reproductive success and survival appeared to be independent of the number of lice or louse flies. Neither parasite correlated with the number, body mass, or date of fledging of young birds, nor with the overwinter survival of adults. We caution, however, that experimental manipulations of parasite load are required for a definitive test of the impact of ectoparasites on evolutionary fitness components.

     

Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama

I investigated the effect of the density of louse eggs (Pedicinus obtusus andP. eurygaster) on grooming site preferences in Japanese macaques (Macaca fuscata). Louse eggs were more often found on the outer side of the body (upper back, lower back, outer arms, and outer legs) than on the inner side of the body (chest, belly, inner arms, and inner legs). Japanese macaques were more likely to be groomed on the outer side than the inner side of the body by allogrooming and autogrooming. Such grooming site preferences correlated with the distribution of louse eggs but not with the areas of body parts. Thus, the ecology of lice might affect grooming behavior of Japanese macaques. Five hundred and fifty louse eggs were estimated to parasitize an adult female Japanese macaque. Considering the intrinsic rate of natural increase of lice, monkeys need to be groomed almost every day. This suggests that Japanese macaques need grooming partners and form social bonds with others for everyday grooming.     

Quantitative observations of grooming behavior in free-rangingMacaca mulatta

Quantitative methods of observation and analysis were used in a 12-month study of grooming behavior of free-rangingMacaca mulatta on La Cueva Island at La Parguera, Puerto Rico. Observations lasting 30–120 minutes were made from eight positions on the island at a standard time of day when monkeys were either feeding or resting. Two dependent variables were obtained: (1) the number of monkeys present in the observation area were noted by age and sex class at five-minute intervals throughout each observation, and (2) the frequency of grooming encounters was tabulated by the age and sex class(es) of groomer and recipient. These data were computed as grooms/hour/possible interacting combination of monkeys. Grooming frequencies were higher in non-feeding situations than when monkeys were feeding. The largest social group had the lowest mean grooming rates, while the smallest group had the highest grooming frequencies. More grooming occurred during the November-to-February mating season than at other periods of the year. Adult females were involved in over 60% of all grooming behavior, juveniles participated in 25% of the grooming, while adult males groomed females, primarily during the mating season, and rarely groomed other males or juveniles. Genealogical relationships, levels of group aggression and the feeding or resting context all influenced the frequency of grooming. This study provides support for the hypothesis that the basic social unit for rhesus macaques consists of a core of adult females with their juvenile and infant progeny.     

How long do louse eggs take to hatch? A possible answer to an age‐old riddle

There are no rigorous data on how long eggs of the head louse, Pediculus capitis (Phthiraptera: Pediculidae), take to hatch. Pediculicide users often report re‐infestations after apparently successful treatments in the absence of infective contacts. This study aimed to resolve the question of whether some louse eggs hatch after the completion of treatment, thereby giving rise to a new infestation. Data were extracted from the records of lice collected after treatments in 20 clinical intervention trials. All datasets were eliminated except those in which only newly hatched louse nymphs were found prior to the final assessment. This excluded the possibility that new eggs were laid after the first treatment and thus any young lice found must have originated from eggs laid before the start of treatment. This identified 23 of 1895 (1.2%) records with evidence of louse nymphs emerging at 13 days or more after the first treatment, 3–6 days longer than previous estimates. Current treatment regimens for pediculicides of two applications 7–10 days apart appear inadequate, which may explain continuing infestation in the community. Therefore, it is suggested that a revised approach using three treatments applied at intervals of 1 week should prevent the survival of any nymphs and their development into a new generation of adults.     

AVIAN BROOD PARASITISM AND ECTOPARASITE RICHNESS–SCALE‐DEPENDENT DIVERSITY INTERACTIONS IN A THREE‐LEVEL HOST–PARASITE SYSTEM

Brood parasitic birds, their foster species and their ectoparasites form a complex coevolving system composed of three hierarchical levels. However, effects of hosts’ brood parasitic life‐style on the evolution of their louse (Phthiraptera: Amblycera, Ischnocera) lineages have never been tested. We present two phylogenetic analyses of ectoparasite richness of brood parasitic clades. Our hypothesis was that brood parasitic life‐style affects louse richness negatively across all avian clades due to the lack of vertical transmission routes. Then, narrowing our scope to brood parasitic cuckoos, we explored macroevolutionary factors responsible for the variability of their louse richness. Our results show that taxonomic richness of lice is lower on brood parasitic clades than on their nonparasitic sister clades. However, we found a positive covariation between the richness of cuckoos’ Ischnoceran lice and the number of their foster species, possibly due to the complex and dynamic subpopulation structure of cuckoo species that utilize several host species. We documented diversity interactions across a three‐level host parasite system and we found evidence that brood parasitism has opposing effects on louse richness at two slightly differing macroevolutionary scales, namely the species richness and the genera richness.     

Immunization of rabbits with a midgut extract of the human body louse Pediculus humanus humanus: the effect of induced resistance on the louse population

Abstract. Resistance to human body lice, Pediculus humanus humanus L, induced by feeding on rabbits immunized with an extract of louse gut was studied. The mortality of lice fed on immunized rabbits was 73%, significantly higher than that of lice fed on control rabbits (52%) ( P < 0.01). The proportion of dead nymphs and female lice with ruptured guts was significantly higher in lice fed on immunized rabbits (P<0.01). The size of the bloodmeal was 35% greater in female lice fed on control rabbits than on immunized rabbits. Lice fed on immunized rabbits laid 40% less eggs than those fed on the controls, they also demonstrated a significant decrease in the number of eggs per female over time ( P < 0.01). 86% of the eggs laid by lice fed on immunized animals hatched, compared with 92% hatching of eggs laid by the lice fed on control animals (P< 0.01). With the exception of the first bloodmeal the percentage of hatched eggs which were laid between any two bloodmeals was significantly smaller (p<0.01) in the lice fed on immunized rabbits than in the control group. The first nymphal stage of lice fed on immunized rabbits took an average of 5.2 days to moult to the second stage, compared with 4 days for those fed on control rabbits.     

The effect of urban and rural habitats and resource type on activity budgets of commensal rhesus macaques (Macaca mulatta) in Bangladesh

Macaques are characterized by their wide distribution and ability to adapt to a variety of habitats. Activity budgets are affected by habitat type, season, and food availability in relation to differing age–sex class and individual requirements. We conducted a comparative study on two commensal rhesus groups, one living in a rural village and the other in the center of urban Dhaka, Bangladesh. The study was conducted in three different seasons between 2007 and 2009 in order to evaluate how habitat type and season affects their behavioral activities. Differences in food type and its availability between these two habitats were mainly responsible for the variations in activity budgets between groups. Feeding time in the rural group was significantly longer than that in the urban group. In contrast, grooming and object manipulation/play were significantly greater in the urban than the rural group. Seasonal variations in all major behaviors were significantly affected by group, with more time spent feeding in summer than in winter/dry season, and more time spent grooming and moving in winter/dry season than summer in the rural group. In contrast, time spent resting was greater in the monsoon and summer seasons than the winter/dry season in the urban group. Grooming time was greater in the winter/dry season than the monsoon and summer seasons. In both groups, immature of both sexes spent significantly more time on feeding and object manipulation/playing and less time resting than adults. Adult females spent more time grooming than males and immatures, of both sexes, in both groups. Moreover, the rural group spent most of their time feeding on garden/crop produce and wild plant food resources, while the urban group spent more time feeding on provisioned foods. These results showed that differences in the activity budgets of rural and urban dwelling macaques were due largely to the differences in available food resources. Commensal rhesus macaques show a high degree of behavioral flexibility in response to habitat and resource variability, and knowledge of these differences is important for the conservation and management of highly commensal primates.     

Molecular phylogeny and novel host associations of avian chewing lice (Insecta: Phthiraptera) from South Africa

Compared with Europe and the Americas, the ectoparasites of African birds are poorly understood, despite the avian fauna being relatively well known. Notably, previous studies documenting the host associations and genetic diversity of parasitic chewing lice of southern African birds have been limited in geographic and taxonomic scope. Recent field expeditions exploring the avian diversity in South Africa facilitated an opportunity to obtain louse specimens from a taxonomically diverse host assemblage. This study is the first to investigate avian louse host associations and diversity across a large portion of South Africa encompassing several distinct habitat types, while incorporating molecular genetic data (from portions of the mitochondrial COI and nuclear EF‐1α genes) for ectoparasite phylogenetic analyses. From 1105 South African bird individuals and 170 species examined for lice, a total of 105 new louse–host associations were observed. Morphological and genetic examination of lice with these new host associations reveals a maximum of 66 louse species new to science. Results of this study support the observation that examining museum specimens is a useful way to investigate louse diversity and host associations.     

灵长类相互理毛的影响因素、功能及其利益分析

理毛行为是动物行为学研究的主要内容之一,根据理毛的对象可分为自我理毛(Autogrooming)和相互理毛(Allogrooming),其中相互理毛是灵长类重要的社会行为。现在认为相互理毛可能与社会参量(亲缘关系、性别、年龄、等级制度、繁殖状况等)有联系,并且有一定的社会功能。本文论述了理毛行为的分类、影响相互理毛的因素、相互理毛功能假说及其相互理毛的投入-收益分析,以便人们对相互理毛的行为进行更深入的研究。     

Sexually and Developmentally Dimorphic Grooming: A Comparative Survey of the Ungulata

Grooming is effective in removing fitness‐compromising ectoparasites, such as ticks. Tick‐removal grooming is regulated both by a central control mechanism (programmed grooming model) and by cutaneous stimulation from tick bites (stimulus‐driven model). The programmed grooming model predicts that organismic factors that impact the cost‐benefit ratio of grooming (e.g., sex and body size) will influence the rate of grooming. The ‘vigilance principle’ predicts that breeding males of sexually dimorphic species will groom less than females to maintain high levels of vigilance for rival males and oestrus females. The intraspecific body size principle predicts that juveniles will engage in more frequent grooming than larger‐bodied adults to compensate for the higher cost of tick infestation for smaller animals. To examine the generalizability of these predictions, we surveyed the grooming rate of 53 species/subspecies of ungulates (primarily Bovidae and Cervidae) in tick‐free zoological parks in which stimulus‐driven grooming was controlled for. Matched‐pair analysis supported both predictions. Males delivered fewer oral grooming episodes per hour than females in 85% of sexually dimorphic species (n = 40), but only 56% of monomorphic species (n = 11) exhibited sexually dimorphic grooming, which was not different from random. Juvenile oral episodes per hour exceeded that of adult females in 74% of surveyed species (n = 36). As predicted by the body size principle, the grooming rate of juveniles declined as juveniles grew larger and less vulnerable to tick infestation. In separate analyses of Bovidae and Cervidae to control for common ancestry, both families supported sexually dimorphic grooming, but developmentally dimorphic grooming was supported only for Bovidae. Our results indicate that sexually dimorphic grooming is widespread in the ungulate species surveyed, suggesting that programmed grooming evolved at least as early as the common ancestor to the Artiodactyla.     

黄山野生短尾猴理毛发生部位的差异

理毛行为是指动物个体用双手或单手从自身或其他个体的毛发中检出颗粒物并放入嘴里咀嚼或直接用嘴进行清理的过程,在灵长类动物社会中普遍存在且频繁发生.本研究以栖息于安徽黄山的野生短尾猴(Macaca thibetana)为研究对象,于2019年7-12月采用目标动物取样法采集行为数据,通过比较自我理毛和社会理毛的发生部位和发...     

云南省吸虱昆虫区系及物种多样性

吸虱是寄生于真兽类哺乳动物体表的专性吸血寄生虫,广布于世界各地。云南省已知吸虱昆虫9科13属44种,分别占中国已知吸虱科、属、种的81.82%,59.09%,45.83%。文章参考大量相关文献,从分类阶元、特有物种、动物地理区划和宿主动物4个方面分析云南省吸虱的物种多样性。云南省吸虱特有种有13种,占云南省已知吸虱种类的29.55%,27种为东洋种,15种为古北和东洋两界兼有种,广布种9种。吸虱在5个地理小区的分布,以横断山中部和横断山南部2个地理小区的吸虱物种多样性较高,其它3个区的物种多样性较低。相对于全国而言,云南省吸虱物种多样性较高,吸虱的宿主动物种类丰富。但蚤、恙螨和革螨等其它体表寄生虫相比较,兽类宿主动物体表吸虱的物种多样性明显低于其它体表寄生虫,1科(属)阶元的吸虱其宿主多为相对一致的1个科(属)动物阶元,反映了吸虱宿主特异性较高的事实,吸虱昆虫与其对应的宿主动物已经形成了比较稳定的"一对一"的寄生关系,这是吸虱昆虫与其宿主动物协同进化的生态学表现。     

Louse infestations of tree shrews (Tupaia glis)

Nine adult tree shrews, Tupaia glis, recently imported from West Malaysia were visually examined for ectoparasites while under general anesthesia. Three shrews were infested by the sucking louse, Sathrax durus , and six shrews had louse ova belonging to this species; two shrews had neither lice nor ova. A total of 20 adult female, 10 adult male, and three third instar nymphal lice was collected. Lice were located on the head, flanks, and dorsal body of shrews while ova were recorded mainly from the anterior flanks but also from some adjacent host sites. The tree shrews appeared to tolerate the lice well although louse vector capacity was not assessed. The last date that lice were recorded from shrews was 22 days after colony set-up, and the last date on which seemingly viable ova were recorded was 64 days after set-up showing that the infestations were ultimately lost.     

Whom to Groom and for What? Patterns of Grooming in Female Barbary Macaques (Macaca sylvanus)

Grooming is one of the most conspicuous social interactions among nonhuman primates. The selection of grooming partners can provide important clues about factors relevant for the distribution of grooming within a social group. We analyzed grooming behavior among 17 semi-free ranging female Barbary macaques (Macaca sylvanus). We tested whether grooming is related to kinship, rank and friendship. Furthermore, we tested whether grooming is reciprocated or exchanged for rank related benefits (i.e. lower aggression and increased tolerance whilst feeding). We found that in general grooming was reciprocally exchanged, directed up the hierarchy and at the same time affected by friendship and kinship. Grooming was more frequent among individuals with higher friendship values as well as amongst related individuals. We also divided our data set on the basis of rank difference and tested if different power asymmetries between individuals affected the tendency to exchange grooming for rank related benefits and grooming reciprocation. In support of our initial hypothesis our results show that the reciprocation of grooming was a significant predictor of grooming interactions between individuals of similar rank, but not between those individuals more distantly separated in the social hierarchy. However, we did not find any evidence for grooming being exchanged for rank related benefits in either data set. Our results, together with previously published studies, illustrate the behavioral flexibility of macaques. It is clear that multiple studies of the same species are necessary to gather the data required for the solid comparative studies needed to shed light on patterns of grooming behavior in primates.     

Impact of external odor on self‐grooming of lesser flat‐headed bats,Tylonycteris pachypus

Grooming is a common behavior of some mammals. Previous studies have shown that grooming is a means by which animals clean themselves, remove ectoparasites, and lower their body temperature. It is also involved in olfactory communication. Bats belong to the order Chiroptera and, like most mammals, are the natural host of many ectoparasites. Bat grooming, including licking and scratching, is one of the ways to reduce the adverse effects caused by ectoparasites. Bat grooming may also be induced by exogenous odor. In this study, we used lesser flat‐headed bats (Tylonycteris pachypus) to test the hypothesis that exogenous odor affects the self‐grooming behavior of bats. Results showed that external odor from distantly related species caused lesser flat‐headed bats to spend more time in self‐grooming. Lesser flat‐headed bats that received odor from humans spent the longest time in self‐grooming, followed by those that received odor from a different species of bats (T. robustula). Lesser flat‐headed bats that received odor form the same species of bats, either from the same or a different colony, spent the least amount of time in self‐grooming. These results suggest that bats can recognize conspecific and heterospecific through body scent.     

Molecular evolution of Pediculus humanus and the origin of clothing

The human head louse (Pediculus humanus capitis) and body louse (P. humanus corporis or P. h. humanus) are strict, obligate human ectoparasites that differ mainly in their habitat on the host : the head louse lives and feeds exclusively on the scalp, whereas the body louse feeds on the body but lives in clothing. This ecological differentiation probably arose when humans adopted frequent use of clothing, an important event in human evolution for which there is no direct archaeological evidence. We therefore used a molecular clock approach to date the origin of body lice, assuming that this should correspond with the frequent use of clothing. Sequences were obtained from two mtDNA and two nuclear DNA segments from a global sample of 40 head and body lice, and from a chimpanzee louse to use as an outgroup. The results indicate greater diversity in African than non-African lice, suggesting an African origin of human lice. A molecular clock analysis indicates that body lice originated not more than about 72,000 +/- 42,000 years ago; the mtDNA sequences also indicate a demographic expansion of body lice that correlates with the spread of modern humans out of Africa. These results suggest that clothing was a surprisingly recent innovation in human evolution.     

Independent origins of the feather lice (Insecta: Degeeriella) of raptors

Although diurnal birds of prey have historically been placed in a single order due to a number of morphological characters, recent molecular phylogenies have suggested that this is a case of convergence rather than homology, with hawks (Accipitridae) and falcons (Falconidae) forming two distantly related groups within birds. The feather lice of birds have often been used as a model for comparing host and parasite phylogenies, and in some cases there is significant congruence between the two. Thus, studying the phylogeny of the lice of diurnal raptors may be of particular interest with respect to the independent evolution of hawks vs. falcons. Using one mitochondrial gene and three nuclear genes, we inferred a phylogeny for the feather louse genus Degeeriella (which are all obligate raptor ectoparasites) and related genera. This phylogeny indicated that Degeeriella is polyphyletic, with lice from falcons vs. hawks forming two distinct clades. Falcon lice were sister to lice from African woodpeckers, whereas Capraiella, a genus of lice from rollers lice, was embedded within Degeeriella from hawks. This phylogeny showed significant geographical structure, with host geography playing a larger role than host taxonomy in explaining louse phylogeny, particularly within clades of closely related lice. However, the louse phylogeny does reflect host phylogeny at a broad scale; for example, lice from the hawk genus Accipiter form a distinct clade. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 837–847.     

Prevalence of patent Baylisascaris procyonis infection in raccoons (Procyon lotor) in Ithaca, New York

The prevalence of patent Baylisascaris procyonis infection in raccoons was determined by examining fecal samples collected between July 1986 and May 1987 in Ithaca, New York. September, October, and November had the highest prevalence of infection (35-48%). Significant differences (P less than 0.001) were found when months were grouped by season to test the hypothesis that a fecal sample's probability of being positive does not vary from month to month. Fall was the season contributing most to the overall chi-square statistic. Host sex/age class and prevalence of patent infection were investigated. The raccoons were aged as either juveniles or adults. A significantly higher prevalence of patent infection (P less than 0.001) was found in juveniles when compared to adults. No statistically significant difference was found in other comparisons of host sex and age. Contingency analysis tested the independence of sex/age class/season and presence of eggs. The results of the test were significant (P less than 0.001).     

Grooming reciprocity in female tibetan macaques macaca thibetana

Grooming among nonhuman primates is widespread and may represent an important service commodity that is exchanged within a biological marketplace. In this study, using focal animal sampling methods, we recorded grooming relationships among 12 adult females in a free-ranging group of Tibetan macaques (Macaca thibetana) at Huangshan, China, to determine the influence of rank and kinship on grooming relationships, and whether females act as reciprocal traders (exchange grooming received for grooming given) or interchange traders (interchange grooming for social tolerance or other commodities). The results showed that: (1) grooming given was positively correlated with grooming received; (2) kinship did not exert a significant influence on grooming reciprocity; and (3) grooming reciprocity occurred principally between individuals of adjacent rank; however, when females of different rank groomed, females tended to groom up the hierarchy (lower ranking individuals groomed higher ranking individuals more than vice versa). Our results support the contention that both grooming reciprocity and the interchange of grooming for tolerance represent important social tactics used by female Tibetan macaques.     

Relative importance of demographics, locale, and seasonality underlying louse and flea parasitism of raccoons (Procyon lotor)

A variety of demographic, seasonal, and site-specific variables may influence parasitism, but the relative importance of these variables is generally unclear. We measured the relative ability of host characteristics, season, and site to explain louse (Trichodectes octomaculatus) and flea (Orchopeas howardi) infestation across 10 populations of raccoons (Procyon lotor). Lice are highly dependent on specific hosts and are predicted to display a relatively strong relationship with factors intrinsic to the host, when compared to fleas, which can infest multiple species and survive off-host for weeks without feeding. We developed a priori models that represented explicit hypotheses and contrasted their ability to predict infestation patterns. While the abundance of lice was seasonal, models that included solely host age and sex best predicted prevalence and abundance, in part because males were infested with 3 times the number of lice than were females. Conversely, flea prevalence and abundance, which peaks sharply in the spring, was best predicted by season; factors intrinsic to the host were relatively unimportant for predicting abundance. These, and other, recent findings emphasize the need to simultaneously assess the relative importance of multiple ecological variables between parasite species when attempting to describe general trends and constraints of host-parasite associations.