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.     

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.     

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.     

Incorporating parasite systematics in comparative analyses of variation in spleen mass and testes sizes of rodents

Parasite diversity is hypothesized to act on host life-history traits through investment in immunity. In order to incorporate the diversity of the parasite community that an individual host or a host species may face, two indices can be used: Taxonomic Species Richness and Taxonomic Entropy, where the taxonomic information is incorporated with the taxonomic weight. We tested whether these indices correlate with several morphological traits potentially implicated in immune defence and in reproduction, using data on gastrointestinal helminths and their rodent hosts sampled in Southeast Asia. We found no relationship between parasite diversity indices and either spleen mass or testes size at the intraspecific level, i.e. at the level of individuals. At the interspecific level, we found no relationship between the parasite diversity indices and testes size. However, we found that female spleen mass is significantly influenced by the specific species richness of parasites, whereas male spleen mass is influenced by individual mean parasite diversity indices. We concluded that female spleen mass may have evolved in response to gastrointestinal helminth pressure acting at species levels, while in males, the individual spleen mass could be constrained by other factors, such as the blood storage function of the spleen.     

Environmental determinants of amphibian and reptile species richness in China

Understanding the factors that regulate geographical variation in species richness has been one of the fundamental questions in ecology for decades, but our knowledge of the cause of geographical variation in species richness remains poor. This is particularly true for herpetofaunas (including amphibians and reptiles). Here, using correlation and regression analyses, we examine the relationship of herpetofaunal species richness in 245 localities across China with 30 environmental factors, which include nearly all major environmental factors that are considered to explain broad-scale species richness gradients in such theories as ambient energy, water–energy dynamics, productivity, habitat heterogeneity, and climatic stability. We found that the species richness of amphibians and reptiles is moderately to strongly correlated with most of the environmental variables examined, and that the best fit models, which include explanatory variables of temperature, precipitation, net primary productivity, minimum elevation, and range in elevation, explain ca 70% the variance in species richness for both amphibians and reptiles after accounting for sample area. Although water and temperature are important explanatory variables to both amphibians and reptiles, water variables explain more variance in amphibian species richness than in reptile species richness whereas temperature variables explain more variance in reptile species richness than in amphibian species richness, which is consistent with different physiological requirements of the two groups of organisms.     

The decoupling of abundance and species richness in lizard communities

1. Patterns of species richness often correlate strongly with measures of energy. The more individuals hypothesis (MIH) proposes that this relationship is facilitated by greater resources supporting larger populations, which are less likely to become extinct. Hence, the MIH predicts that community abundance and species richness will be positively related. 2. Recently, Buckley & Jetz (2010, Journal of Animal Ecology, 79, 358-365) documented a decoupling of community abundance and species richness in lizard communities in south-west United States, such that richer communities did not contain more individuals. They predicted, as a consequence of the mechanisms driving the decoupling, a more even distribution of species abundances in species-rich communities, evidenced by a positive relationship between species evenness and species richness. 3. We found a similar decoupling of the relationship between abundance and species richness for lizard communities in semi-arid south-eastern Australia. However, we note that a positive relationship between evenness and richness is expected because of the nature of the indices used. We illustrate this mathematically and empirically using data from both sets of lizard communities. When we used a measure of evenness, which is robust to species richness, there was no relationship between evenness and richness in either data set. 4. For lizard communities in both Australia and the United States, species dominance decreased as species richness increased. Further, with the iterative removal of the first, second and third most dominant species from each community, the relationship between abundance and species richness became increasingly more positive. 5. Our data support the contention that species richness in lizard communities is not directly related to the number of individuals an environment can support. We propose an alternative hypothesis regarding how the decoupling of abundance and richness is accommodated; namely, an inverse relationship between species dominance and species richness, possibly because of ecological release.     

Assessing conservation value of stream communities: a comparison of approaches based on centres of density and species richness

1. We used a recently developed Index of Centres of Density (ICD) to assess conservation value of thirty-nine sites in the upper Clinch River drainage of Virginia and Tennessee, U.S.A. The ICD incorporates information on the population density of each species at a site relative to sites throughout the region.
2. Value assessments based on the ICD were compared to those based on species richness. Species richness at sites was not related to ICD scores, but collective species lists from high-ranking sites were similar for both approaches. All sites with rare species had either a high ICD score or high species richness.
3. Four community types (defined by physiography and stream size) were better represented in sites with high-ranking ICDs than in sites with high-ranking species richness. Sites with high ICD scores were distributed uniformly throughout the region.
4. The ICD is a more powerful tool than species richness for assessing conservation value because the ICD identifies areas with regionally rare species, especially viable populations, or distinctive communities, all of which are key components of a region's biodiversity.     

Insights from comparative analyses of aging in birds and mammals

Many laboratory models used in aging research are inappropriate for understanding senescence in mammals, including humans, because of fundamental differences in life history, maintenance in artificial environments, and selection for early aging and high reproductive rate. Comparative studies of senescence in birds and mammals reveal a broad range in rates of aging among a variety of taxa with similar physiology and patterns of development. These comparisons suggest that senescence is a shared property of all vertebrates with determinate growth, that the rate of senescence has been modified by evolution in response to the potential life span allowed by extrinsic mortality factors, and that most variation among species in the rate of senescence is independent of commonly ascribed causes of aging, such as oxidative damage. Individuals of potentially long‐lived species, particularly birds, appear to maintain high condition to near the end of life. Because most individuals in natural populations of such species die of aging‐related causes, these populations likely harbor little genetic variation for mechanisms that could extend life further, or these mechanisms are very costly. This, and the apparent evolutionary conservatism in the rate of increase in mortality with age, suggests that variation in the rate of senescence reflects fundamental changes in organism structure, likely associated with the rate of development, rather than physiological or biochemical processes influenced by a few genes. Understanding these evolved differences between long‐lived and short‐lived organisms would seem to be an essential foundation for designing therapeutic interventions with respect to human aging and longevity.     

Effect of habitat complexity on population density and species richness in tropical intertidal predatory gastropod assemblages

Summary Structural complexity of the habitat significantly increases population density and number of species in assemblages of predatory gastropod molluscs (families Conidae, Muricidae, Mitridae and Vasidae) on intertidal, generally smooth, horizontal limestone platforms fringing tropical Pacific islands. The important topographic features are physical (depressions partly filled with coral rubble) and biotic (thick algal turf binding sand). Higher population density and species richness in areas with than without such natural refuges, and following experimental addition of artificial refuges on portions of habitat lacking them support this hypothesis. Two species of Drupa differ from the other species present in not utilizing refuges during times of physical stress; this is attributed to their depressed shell and broad, tenacious foot. Highest gastropod densities occur in steep-sided depressions and those containing much coral rubble and sand, suggesting that these are important qualities of refuges. We believe this is the first demonstration of how specific environmental factors affect population density and species diversity of benthic invertebrates in a coral reef-associated habitat.     

Functional richness, functional evenness, and use of niche space in parasite communities

Most efforts aimed at elucidating the factors responsible for the variation in species richness among different parasite communities have focused on host characteristics such as body mass or diet. Independently of host features, however, the way in which parasites use resources within the host may also affect the species richness of the community. The distribution of parasite individuals or biomass in niche space determines whether host resources are used evenly, or whether there are gaps in resource use, with some parts of the total niche being underutilized. Here, the concepts of functional richness and functional evenness are applied to parasite communities for the first time, using simple indices. Measurements of the distribution of species in niche space within communities, such as mapping the distribution of helminths along the length of the host's intestine, is standard practice in parasitology. In such cases, functional richness is simply the proportion of the total number of intestine sections available that are used by at least 1 worm, whereas functional evenness measures the evenness in the distribution of worm numbers or biomass across all niche sections that are occupied. Data on cestode communities of elasmobranchs are used to illustrate the use of these indices, and to show how important they can be in tests of ecological hypotheses. The indices presented here capture essential features of resource use in parasite communities, and can be useful tools for comparative analyses.     

Modelling species richness and diversity in grassland communities of the Central Caucasus

In this study I used small squares (4 cm×4 cm) as a sampling technique within plots (128 cm×128 cm) of different elevation, aspect and slope angle in grassland communities (20 plots examined). Then I used a rectangular hyperbole equation (the Michaelis-Menten model) to describe species richness and the Inverse of Simpson Concentration (ISC) as functions of sample size. I checked robustness and precision of the model both by interpolation and extrapolation. Interpolation was similarly good in both cases, while extrapolation produced reliable predictions of ISC but underestimated species richness. Dominance analysis indicated that the underestimation of richness depends on the proportion of bottom species, and that the predicted values of richness roughly coincide with the numbers of dominant species found in plots. Therefore, the model may be used to assess number of dominant species when precision is less important than saving time during a survey. However, the rectangular hyperbole equation appears to be precise and robust in the prediction of ISC, at least in grassland communities. This property may also be employed for extrapolation of diversity indices with a limited sampling effort.