Host longevity and parasite species richness in mammals

Hosts and parasites co-evolve, with each lineage exerting selective pressures on the other. Thus, parasites may influence host life-history characteristics, such as longevity, and simultaneously host life-history may influence parasite diversity. If parasite burden causes increased mortality, we expect a negative association between host longevity and parasite species richness. Alternatively, if long-lived species represent a more stable environment for parasite establishment, host longevity and parasite species richness may show a positive association. We tested these two opposing predictions in carnivores, primates and terrestrial ungulates using phylogenetic comparative methods and controlling for the potentially confounding effects of sampling effort and body mass. We also tested whether increased host longevity is associated with increased immunity, using white blood cell counts as a proxy for immune investment. Our analyses revealed weak relationships between parasite species richness and longevity. We found a significant negative relationship between longevity and parasite species richness for ungulates, but no significant associations in carnivores or primates. We also found no evidence for a relationship between immune investment and host longevity in any of our three groups. Our results suggest that greater parasite burden is linked to higher host mortality in ungulates. Thus, shorter-lived ungulates may be more vulnerable to disease outbreaks, which has implications for ungulate conservation, and may be applicable to other short-lived mammals.     

Density, body mass and parasite species richness of terrestrial mammals

We investigated the relationships between helminth species richness and body mass and density of terrestrial mammals. Cross-species analysis and the phylogenetically independent contrast method produced different results. A non-phylogenetic approach (cross-species comparisons) led to the conclusion that parasite richness is linked to host body size. However, an analysis using phylogenetically independent contrasts showed no relationship between host body size and parasite richness. Conversely, a non-phylogenetic approach generated a negative relationship between parasite richness and host density, whereas the independent contrast method showed the opposite trend – that is, parasite richness is positively correlated with host density. From an evolutionary perspective, our results suggest that opportunities for parasite colonization depend more closely on how many hosts are available in a given area than on how large the hosts are. From an epidemiological point of view, our results confirm theoretical models which assume that host density is linked to the opportunity of a parasite to invade a population of hosts. Our findings also suggest that parasitism may be a cost associated with host density. Finally, we provide some support for the non-linear allometry between density and mammal body mass (Silva and Downing, 1995), and explain why host density and host body mass do not relate equally to parasite species richness.     

Host densities as determinants of abundance in parasite communities

Several epidemiological models predict a positive relationship between host population density and abundance of directly transmitted macroparasites. Here, we generalize these, and test the prediction by a comparative study. We used data on communities of gastrointestinal strongylid nematodes from 19 mammalian species, representing examination of 6670 individual hosts. We studied both the average abundance of all strongylid nematodes within a host species, and the two components of abundance, prevalence and intensity. The effects of host body weight, diet, fecundity and age at maturity and parasite body size were controlled for directly, and the phylogenetically independent contrast method was used to control for confounding factors more generally. Host population density and average parasite abundance were strongly positively correlated within mammalian taxa, and across all species when the effects of host body weight were controlled for. Controlling for other variables did not change this. Even when looking at single parasite species occurring in several host species, abundance was highest in the host species with the highest population density. Prevalence and intensity showed similar patterns. These patterns provide the first macroecological evidence consistent with the prediction that transmission rates depend on host population density in natural parasite communities.     

Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla

Host social, ecological and life history traits are predicted to influence both parasite establishment within host species and the distribution of parasites among host species. Yet only a few studies have investigated the role multiple host traits play in determining patterns of infection across diverse parasite groups. To explore the association between host traits and parasite species richness (PSR), we assembled a comprehensive database encompassing 601 parasites (including viruses, bacteria, protozoa, helminths and arthropods) reported to infect 96 species from two well-studied and diverse host clades: even- and odd-toed hoofed mammals (Artiodactyla and Perissodactyla). Comparative analyses were used to examine associations between three sets of host variables (life history and body mass, social and mating behavior, and ecological traits) and PSR for all parasites combined and for distinct parasite sub-groups. Results from a combination of phylogenetic and non-phylogenetic tests showed that PSR increased with host body size across all parasites groups. Counter to expectations, measures of parasite diversity decreased with host longevity and social group size, and associations between group size and PSR further depended on the underlying mating system of the host species. Our results suggest that body mass, longevity, and social organization influence the diversity and types of parasites reported to infect wild populations of hoofed mammals, and that multiple host and parasite traits can combine in unexpected ways to shape observed patterns.     

Helminth species diversity of mammals: parasite species richness is a host species attribute

Studies investigating parasite diversity have shown substantial geographical variation in parasite species richness. Most of these studies have, however, adopted a local scale approach, which may have masked more general patterns. Recent studies have shown that ectoparasite species richness in mammals seems highly repeatable among populations of the same mammal host species at a regional scale. In light of these new studies we have reinvestigated the case of parasitic helminths by using a large data set of parasites from mammal populations in 3 continents. We collected homogeneous data and demonstrated that helminth species richness is highly repeatable in mammals at a regional scale. Our results highlight the strong influence of host identity in parasite species richness and call for future research linking helminth species found in a given host to its ecology, immune defences and potential energetic trade-offs.     

Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density

Aim  Comparative studies have revealed strong links between ecological factors and the number of parasite species harboured by different hosts, but studies of different taxonomic host groups have produced inconsistent results. As a step towards understanding the general patterns of parasite species richness, we present results from a new comprehensive data base of over 7000 host–parasite combinations representing 146 species of carnivores (Mammalia: Carnivora) and 980 species of parasites.
Methods  We used both phylogenetic and non-phylogenetic comparative methods while controlling for unequal sampling effort within a multivariate framework to ascertain the main determinants of parasite species richness in carnivores.
Results  We found that body mass, population density, geographical range size and distance from the equator are correlated with overall parasite species richness in fissiped carnivores. When parasites are classified by transmission mode, body mass and home range area are the main determinants of the richness of parasites spread by close contact between hosts, and population density, geographical range size and distance from the equator account for the diversity of parasites that are not dependent on close contact. For generalist parasites, population density, geographical range size and latitude are the primary predictors of parasite species richness. We found no significant ecological correlates for the richness of specialist or vector-borne parasites.
Main conclusions  Although we found that parasite species richness increases instead of decreases with distance from the equator, other comparative patterns in carnivores support previous findings in primates, suggesting that similar ecological factors operate in both these independent evolutionary lineages.     

The relationship between species richness and productivity in metazoan parasite communities

Biodiversity is not distributed homogeneously in space, and it often covaries with productivity. The shape of the relationship between diversity and productivity, however, varies from a monotonic linear increase to a hump-shaped curve with maximum diversity values corresponding to intermediate productivity. The system studied and the spatial scale of study may affect this relationship. Parasite communities are useful models to test the productivity-diversity relationship because they consist of species belonging to a restricted set of higher taxa common to all host species. Using total parasite biovolume per host individual as a surrogate for community productivity, we tested the relationship between productivity and species richness among assemblages of metazoan parasites in 131 vertebrate host species. Across all host species, we found a linear relationship between total parasite biovolume and parasite species richness, with no trace of a hump-shaped curve. This result remained after corrections for the potential confounding effect of the number of host individuals examined per host species, host body mass, and phylogenetic relationships among host species. Although weaker, the linear relationship remained when the analyses were performed within the five vertebrate groups (fish, amphibians, reptiles, mammals and birds) instead of across all host species. These findings agree with the classic isolationist-interactive continuum of parasite communities that has become widely accepted in parasite ecology. They also suggest that parasite communities are not saturated with species, and that the addition of new species will result in increased total parasite biovolume per host. If the number of parasite species exploiting a host population is not regulated by processes arising from within the parasite community, external factors such as host characteristics may be the main determinants of parasite diversity.     

Interspecific allometry of population density in mammals and other animals: the independence of body mass and population energy-use

Global regressions of ecological population densities on body mass for mammals and for terrestrial animals as a whole show that local population energy-use is approximately independent of adult body mass—over a body mass range spanning more than 11 orders of magnitude. This independence is represented by the slope of the regressions approximating –0.75, the reciprocal of the way that individual metabolic requirements scale with body mass. The pattern still holds for mammalian primary consumers when the data are broken down by geographic area, by broad habitat-type and by individual community. Slopes for mammalian secondary consumers are also not statistically distinguishable from –0.75. For any given body mass temperate herbivores maintain on average population densities of 1.5 to 2.0 times those of tropical ones, though slopes do not differ. Terrestrial animals of all sizes exhibit approximately the same range of population energy-use values. These results agree with those reported for population energy-budgets. It is suggested that rough independence of body mass and the energy-use of local populations is a widespread rule of animal ecology and community structure.     

Generic species richness and body mass in North American mammals: Support for the inverse relationship of body size and speciation rate

Generic species richness, the number of species per genus, is examined as a function of mean generic body mass for extant North American mammals. Species richness decreases as an inverse power function with increased mass, and the Spearman rank correlation coefficient of the logio transformed data is significant (r_s= ‐0.37). When the data are partitioned by trophic level, the relationship is not statistically significant for carnivores but strengthens for herbivores (r_s= ‐0.46). This interesting but incidental effect is due to the negligible number of diminutive and excessively large carnivores, which is in turn determined by foraging strategies. Alternate hypotheses for the “right‐skewed”; size distribution of modern North American mammals, such as disproportionate extinction of large species, differential species longevity, and a geographical scaling function, are rejected in favor of the proposition that elevated levels of speciation are restricted to animals of small body mass, as originally proposed by Gould and Eldredge (1977). This phenomenon is explained as a function of habitat restriction and particularly in herbivores, limited home range size. Aquatic mammals, regardless of body size, speciate rarely. Cope's Rule, the tendency of many animal groups to evolve towards large size, is understood as a probabilistic statement reflecting the phylogenetic tendencies of a disproportionately high number of small species alive at any given point in time.     

Host ecology and life-history traits associated with blood parasite species richness in birds

Identifying host traits associated with the number of different parasite species or strains harboured by a particular host species can have important implications for understanding the impact of parasitism on hosts. We investigated associations between host ecology and life history, and parasite richness and prevalence of the four major avian blood parasite genera. We used an extensive data on blood parasite infections and host ecology in 263 bird species from the Western Palearctic, combining species-specific data with a comparative approach to control for similarity in phenotype among host species due to the effects of common phylogenetic descent. Adult survival rate negatively correlated with the number of parasite species infecting a host species when controlling for similarity due to common descent and body mass. In addition, the prevalence of Haemoproteus, Plasmodium and Leucocytozoon was higher in species harbouring a richer parasite assemblage. These results suggest that the impact on host fitness caused by avian haematozoa may be underestimated in natural populations if the exacerbated virulence associated with exposure to multiple parasites is not taken into account.     

Riparian bryophyte communities on Madeira: patterns and determinants of species richness and composition

Abstract

We studied 16 streams evenly distributed over the northern and southern slopes of Madeira in order to investigate the riparian bryoflora. Within each stream, three positions (upper, middle and lower reaches) were delimited and within each position two areas were selected. Within each area two plots (each composed of six microplots of 0.2 m²) were sampled, one in the within-stream habitat (submerged all year round), and the other in the stream-border habitat (submerged only in winter). We found that species composition of the riparian bryophytes is affected by the habitat and position in the stream, but not by the main aspect (northern versus southern slope). Concerning species richness, we found that the stream-border community was clearly richer than the within-stream community, upstream plots were richer than plots downstream, and plots on the northern slope of the island were richer than plots on the southern slope. Habitat type was the most significant factor in determining the richness of the threatened species with more species present in the stream-border habitat. Additive partitioning showed that the between-stream component contributed most to total species richness, especially to the richness of the infrequent and threatened species. However, for the common species, the lowest level, i.e. the within-area component, was the most important. Although northern upstream areas are climatically favourable for many bryophyte species due to their higher humidity, the clear effects found may not only be climate-induced, as these areas are also less disturbed and mostly covered by the natural laurel forest. In the southern, downstream parts only a few species were present. Human impacts are largest in the latter situations and probably contributed to the low species richness. As the streams differed considerably in terms of their bryophyte flora, and most of the species were rare, changes in the riparian areas can greatly affect the bryoflora. Therefore, in order to protect the riparian bryophytes as comprehensively as possible, we emphasize the need for careful monitoring of any changes.     

Correlates of species richness in mammals: body size, life history, and ecology

We present the most extensive examination to date of proposed correlates of species richness. We use rigorous phylogenetic comparative techniques, data for 1,692 mammal species in four clades, and multivariate statistics to test four hypotheses about species richness and compare the evidence for each. Overall, we find strong support for the life-history model of diversification. Species richness is significantly correlated with shorter gestation period in the carnivores and large litter size in marsupials. These traits and short interbirth intervals are also associated with species richness in a pooled analysis of all four clades. Additionally, we find some support for the abundance hypotheses in different clades of mammals: abundance correlates positively with species richness in primates but negatively in microchiropterans. Our analyses provide no evidence that mammalian species richness is associated with body size or degree of sexual dimorphism.     

Body mass, population density, and offspring number in mammals

The negative relationship between population density and body mass with the body mass exponent of -0.75 implies that the energy flow through populations of small- and large-bodied species is the same, for individual metabolism scales to body mass raised to the power of +0.75. This relationship called the energetic equivalence rule, has often been observed for mammal species assemblages studied at regional scales. Here we suggest a demography-based mechanism that may generate it. Having analyzed about 130 literature sources, mostly in Russian, we collected demography and body-mass data for 88 mammalian species from the territory and coastal waters of the former Soviet Union. The data were used to construct a number of interspecific relationships. It is shown that (1) the number of offspring per lifetime is approximately inversely proportional to the relative mass at birth (the exponent is not significantly different from -1), (2) the average lifespan is proportional to body mass to the 0.25 power, (3) body mass at birth is proportional to the adult body mass. We develop a simple theory to demonstrate that relations (1) to (3) entail the energetic equivalence rule. The theory also allows us to explain violation of this rule (in non-flying birds, for example), namely, to predict the exponent of relation (1) for any given exponent of the relation between population density and body mass. This is possible because relations (2) and (3) are likely to more universally hold than relation (1). Finally, since natural selection acts on individual traits rather than on population-level ones such as population density, the theory opens up the way to an evolutionary explanation for the energetic equivalence rule.     

A comparative study of migratory behaviour and body mass as determinants of moult duration in passerines

Birds moult to maintain plumage function through life, but the factors that determine moult duration are poorly understood. In temperate areas, variation in moult duration could be largely associated with between-species differences in migratory behaviour (migrants have less time for moulting after breeding), and body mass (because the aerodynamic cost of rapid moult increases allometrically with body size). Moreover, if the energetic cost of transport favours a smaller body size in migratory species, then the effects of migratory behaviour and body mass on moult duration could be confounded. We conducted a comparative study of the duration of adult complete moult in 48 European passerine species, in relation to body mass and migratory behaviour (sedentary, short-distance migrants and long-distance migrants). Lighter and more migratory species moulted faster than heavier and more sedentary species, but migration was not associated with body mass. If accelerated moult compromises the success of migration, changes in the physiology or phenology of moult in migratory birds are better interpreted as adaptive responses to compensate for such costs.     

Host diversity and environmental variables as determinants of the species richness of the parasitoids of leaf‐cutting ants

Aim Because of the obligatory relationship between endoparasitoids and their hosts, we presume that hosts exert strong selection pressure on parasitoids. One prediction is a positive relationship between host diversity and parasitoid richness. This relationship could be the product of resource availability which could lead to more opportunities for speciation, or could represent shared responses to the environment by both groups. Location Argentina and Paraguay. Methods We sampled a 1800‐km transect to test for a correlation between the richness of leaf‐cutting ant hosts and their phorid parasitoids. Regression models were used to assess if host and environmental variables could explain phorid species richness at nest, hectare and locality spatial scales. We used canonical correspondence analysis (CCA) to explore if there were similar responses of phorid species to particular host and environmental variables at different spatial scales, and partial CCA to separate the relative importance of both groups of variables. Results Phorid richness was positively correlated with host richness. Host richness/abundance accounted for 20–53% of the variation in parasitoid richness at the hectare and locality scales of analysis, with most of the variation accounted for by ant abundance. We were not able to assess the prediction at the nest scale as only one phorid species was found at most nests. Climatic variables did not explain phorid species richness once host variables were in the models. Partial CCA showed that host‐related variables accounted for most of the variance associated with phorid species ordination at the nest and hectare scales, but not at the largest grain, the locality, where climatic variables were more important. However, most phorid species did not show particular positions along the climatic gradient. Main conclusions The association between parasitoid richness and host richness and abundance, and the overall weak associations with environmental variables, suggest that these host variables are key factors influencing parasitoid speciation.     

West African rivers as biogeographic islands: species richness of fish communities

Summary Some factors influencing the species richness of West African fish communities were studied in a sample of 26 rivers using four habitat and hydrologic variables. Analysis of a larger sample of 39 rivers showed that species richness was positively related to area. A power function with an exponent of 0.32 gave the best fit. As the surface area used was that of the catchment area and not that (unknown) of the river, the biological significance of this relationship and the possibilities of comparison were limited. Ridge regression analysis and forward stepwise selection indicated that a model that explained ln(species richness) as a function of ln(mean annual discharge) and ln-(catchment surface area) was best, accounting for 90% of the variance of the dependent variable. The combination of surface area and discharge was presumed to act through the volume of water available for the fishes and habitat productivity. Habitat diversity, measured by the diversity of the terrestrial vegetation covering the catchment area, had no significant positive effect when surface area was used in the regression. Rivers (islands) should have fewer species than tributaries of similar size since, for fishes within a river system (continent), there is free circulation between all its branches. The model derived from the river data underestimated the species richness of a sample of 11 tributaries. This was compatible with the hypothesis of higher population extinction rates in insular biotopes. The residuals of the linear model did not show random geographical distribution; the rivers in some areas had more species than expected. The possibility that historical factors, especially Quaternary climatic variations, might cause this distribution is discussed.     

Brief communication: Hair density and body mass in mammals and the evolution of human hairlessness

Humans are unusual among mammals in appearing hairless. Several hypotheses propose explanations for this phenotype, but few data are available to test these hypotheses. To elucidate the evolutionary history of human “hairlessness,” a comparative approach is needed. One previous study on primate hair density concluded that great apes have systematically less dense hair than smaller primates. While there is a negative correlation between body size and hair density, it remains unclear whether great apes have less dense hair than is expected for their body size. To revisit the scaling relationship between hair density and body size in mammals, I compiled data from the literature on 23 primates and 29 nonprimate mammals and conducted Phylogenetic Generalized Least Squares regressions. Among anthropoids, there is a significant negative correlation between hair density and body mass. Chimpanzees display the largest residuals, exhibiting less dense hair than is expected for their body size. There is a negative correlation between hair density and body mass among the broader mammalian sample, although the functional significance of this scaling relationship remains to be tested. Results indicate that all primates, and chimpanzees in particular, are relatively hairless compared to other mammals. This suggests that there may have been selective pressures acting on the ancestor of humans and chimpanzees that led to an initial reduction in hair density. To further understand the evolution of human hairlessness, a systematic study of hair density and physiology in a wide range of species is necessary. Am J Phys Anthropol 152:145–150, 2013. © 2013 Wiley Periodicals, Inc.     

Causes and consequences of variation in offspring body mass: meta‐analyses in birds and mammals

Early survival is highly variable and strongly influences observed population growth rates in most vertebrate populations. One of the major potential drivers of survival variation among juveniles is body mass. Heavy juveniles are better fed and have greater body reserves, and are thus assumed to survive better than light individuals. In spite of this, some studies have failed to detect an influence of body mass on offspring survival, questioning whether offspring body mass does indeed consistently influence juvenile survival, or whether this occurs in particular species/environments. Furthermore, the causes for variation in offspring mass are poorly understood, although maternal mass has often been reported to play a crucial role. To understand why offspring differ in body mass, and how this influences juvenile survival, we performed phylogenetically corrected meta‐analyses of both the relationship between offspring body mass and offspring survival in birds and mammals and the relationship between maternal mass and offspring mass in mammals. We found strong support for an overall positive effect of offspring body mass on survival, with a more pronounced influence in mammals than in birds. An increase of one standard deviation of body mass increased the odds of offspring survival by 71% in mammals and by 44% in birds. A cost of being too fat in birds in terms of flight performance might explain why body mass is a less reliable predictor of offspring survival in birds. We then looked for moderators explaining the among‐study differences reported in the intensity of this relationship. Surprisingly, sex did not influence the intensity of the offspring mass–survival relationship and phylogeny only accounted for a small proportion of observed variation in the intensity of that relationship. Among the potential factors that might affect the relationship between mass and survival in juveniles, only environmental conditions was influential in mammals. Offspring survival was most strongly influenced by body mass in captive populations and wild populations in the absence of predation. We also found support for the expected positive effect of maternal mass on offspring mass in mammals (r_pearson = 0.387). As body mass is a strong predictor of early survival, we expected heavier mothers to allocate more to their offspring, leading them to be heavier and so to have a higher survival. However, none of the potential factors we tested for variation in the maternal mass–offspring mass relationship had a detectable influence. Further studies should focus on linking these two relationships to determine whether a strong effect of offspring size on early survival is associated with a high correlation coefficient between maternal mass and offspring mass.