Parental energy expenditure: a proximate cause of helper recruitment in the pied kingfisher (Ceryle rudis)

Summary Energy expenditure of adult Pied Kingfishers was measured with doubly-labeled water. Results were related to reproductive success of parents aided and unaided by helpers. Energetically stressed parents in a colony with poor food supply accepted potential helpers more often than unstressed birds in another colony where food was easily available. This treatment of helpers was reversed in both colonies through experimental manipulation of clutch size and hence energetic stress. Results are discussed in relation to the costs and benefits that helpers incur on the parents' fitness.     

Globalization of human infectious disease

Globalization has facilitated the spread of numerous infectious agents to all corners of the planet. Analysis of the Global Infectious Disease and Epidemiology Network (GIDEON) database quantitatively illustrates that the globalization of human infectious agents depends significantly on the range of hosts used. Infectious agents specific to humans are broadly and uniformly distributed, whereas zoonotic infectious agents are far more localized in their geographical distribution. Moreover, these patterns vary depending on transmission mode and infectious agent taxonomy. This dichotomy is unlikely to persist if certain aspects of globalization (for example, exotic species introductions) continue unabated. This raises a serious concern for public health and leaves nations with the task of determining the infectious agents that have the greatest potential to establish within their borders. At the advent of a century characterized by an apparent increase in emerging infectious diseases, these results have critical implications for public-health policy and future research pathways of infectious disease ecology.     

Emerging prion disease drives host selection in a wildlife population

Infectious diseases are increasingly recognized as an important force driving population dynamics, conservation biology, and natural selection in wildlife populations. Infectious agents have been implicated in the decline of small or endangered populations and may act to constrain population size, distribution, growth rates, or migration patterns. Further, diseases may provide selective pressures that shape the genetic diversity of populations or species. Thus, understanding disease dynamics and selective pressures from pathogens is crucial to understanding population processes, managing wildlife diseases, and conserving biological diversity. There is ample evidence that variation in the prion protein gene (PRNP) impacts host susceptibility to prion diseases. Still, little is known about how genetic differences might influence natural selection within wildlife populations. Here we link genetic variation with differential susceptibility of white-tailed deer to chronic wasting disease (CWD), with implications for fitness and disease-driven genetic selection. We developed a single nucleotide polymorphism (SNP) assay to efficiently genotype deer at the locus of interest (in the 96th codon of the PRNP gene). Then, using a Bayesian modeling approach, we found that the more susceptible genotype had over four times greater risk of CWD infection; and, once infected, deer with the resistant genotype survived 49% longer (8.25 more months). We used these epidemiological parameters in a multi-stage population matrix model to evaluate relative fitness based on genotype-specific population growth rates. The differences in disease infection and mortality rates allowed genetically resistant deer to achieve higher population growth and obtain a long-term fitness advantage, which translated into a selection coefficient of over 1% favoring the CWD-resistant genotype. This selective pressure suggests that the resistant allele could become dominant in the population within an evolutionarily short time frame. Our work provides a rare example of a quantifiable disease-driven selection process in a wildlife population, demonstrating the potential for infectious diseases to alter host populations. This will have direct bearing on the epidemiology, dynamics, and future trends in CWD transmission and spread. Understanding genotype-specific epidemiology will improve predictive models and inform management strategies for CWD-affected cervid populations.     

Expansion of a central California kelp forest following the mass mortality of sea urchins

The mass mortality by disease of a localized population of sea urchins, Strongylocencrotus franciscanus, on the seaward side of a kelp forest was followed by the rapid seaward expansion of 4 species of brown algae, Macrocystis pyrifera, Laminaria dentigera, Pterygophora california, and to a lesser extent, Nereocystis leutkeana. One other brown alga, Cystoseira osmundacea, failed to become established in the newly available area. Competition among M. pyrifera, L. dentigera, P. californica, and N. Leutkeana apparently was severe, and within 1 year after the demise of the sea urchins, M. pyrifera formed a dense, nearly monospecific stand. Experimental removal of M. pyrifera demonstrated that the canopy of these plants limited light penetration to levels below that necessary for the growth and survival of other brown and red algae.     

Reservoir‐host amplification of disease impact in an endangered amphibian

Emerging wildlife pathogens are an increasing threat to biodiversity. One of the most serious wildlife diseases is chytridiomycosis, caused by the fungal pathogen, Batrachochytrium dendrobatidis (Bd), which has been documented in over 500 amphibian species. Amphibians vary greatly in their susceptibility to Bd; some species tolerate infection, whereas others experience rapid mortality. Reservoir hosts—species that carry infection while maintaining high abundance but are rarely killed by disease—can increase extinction risk in highly susceptible, sympatric species. However, whether reservoir hosts amplify Bd in declining amphibian species has not been examined. We investigated the role of reservoir hosts in the decline of the threatened northern corroboree frog (Pseudophryne pengilleyi) in an amphibian community in southeastern Australia. In the laboratory, we characterized the response of a potential reservoir host, the (nondeclining) common eastern froglet (Crinia signifera), to Bd infection. In the field, we conducted frog abundance surveys and Bd sampling for both P. pengilleyi and C. signifera. We built multinomial logistic regression models to test whether Crinia signifera and environmental factors were associated with P. pengilleyi decline. C. signifera was a reservoir host for Bd. In the laboratory, many individuals maintained intense infections (>1000 zoospore equivalents) over 12 weeks without mortality, and 79% of individuals sampled in the wild also carried infections. The presence of C. signifera at a site was strongly associated with increased Bd prevalence in sympatric P. pengilleyi. Consistent with disease amplification by a reservoir host, P. pengilleyi declined at sites with high C. signifera abundance. Our results suggest that when reservoir hosts are present, population declines of susceptible species may continue long after the initial emergence of Bd, highlighting an urgent need to assess extinction risk in remnant populations of other declined amphibian species.     

Model of coral population response to accelerated bleaching and mass mortality in a changing climate

We model coral community response to bleaching and mass mortality events which are predicted to increase in frequency with climate change. The model was parameterized for the Arabian/Persian Gulf, but is generally applicable. We assume three species groups (Acropora, faviids, and Porites) in two life-stages each where the juveniles are in competition but the adults can enter a size-refuge in which they cannot be competitively displaced. An aggressive group (Acropora species) dominates at equilibrium, which is not reached due to mass mortality events that primarily disadvantage this group (compensatory mortality, >90% versus 25% in faviids and Porites) roughly every 15 years. Population parameters (N individuals, carrying capacity) were calculated from satellite imagery and in situ transects, vital rates (fecundity, mortality, and survival) were derived from the model, field observations, and literature. It is shown that populations and unaltered community structure can persist despite repeated 90% mortality, given sufficiently high fecundity of the remaining population or import from connected populations. The frequency of disturbance determines the dominant group—in low frequency Acropora, in high frequency Porites. This is congruent with field observations. The model of an isolated population was more sensitive to parameter changes than that of connected populations. Highest sensitivity was to mortality rate and recruitment rate. Community composition was sensitive to spacing of disturbances and level of catastrophic mortality. Decreased mortality led to Acropora dominance, increased mortality led to Acropora extinction. In nature, closely spaced disturbances have severely disadvantaged Acropora populations over the last decade. Unless a longer (>10 years) disturbance-free interval can be maintained, a permanent shift away from Acropora dominance will be observed. A mortality rate of 99% in Acropora, as observed in 1996, is not sustainable if repetitive and neither is a disturbance frequency <15 years—each leading to population collapse. This shows that the severity and/or the spacing of the 1996–1998–2002 disturbances were unusual in frequency and duration.     

Life-history trade-offs influence disease in changing climates: strategies of an amphibian pathogen

Life-history trade-offs allow many animals to maintain reproductive fitness across a range of climatic conditions. When used by parasites and pathogens, these strategies may influence patterns of disease in changing climates. The chytrid fungus, Batrachochytrium dendrobatidis, is linked to global declines of amphibian populations. Short-term growth in culture is maximal at 17 degrees-25 degrees C. This has been used in an argument that global warming, which increases the time that amphibians spend at these temperatures in cloud-covered montane environments, has led to extinctions. Here we show that the amphibian chytrid responds to decreasing temperatures with trade-offs that increase fecundity as maturation rate slows and increase infectivity as growth decreases. At 17 degrees-25 degrees C, infectious zoospores encyst (settle and develop a cell wall) and develop into the zoospore-producing stage (zoosporangium) faster, while at 7 degrees-10 degrees C, greater numbers of zoospores are produced per zoosporangium; these remain infectious for a longer period of time. We modeled the population growth of B. dendrobatidis through time at various temperatures using delayed differential equations and observational data for four parameters: developmental rate of thalli, fecundity, rate of zoospore encystment, and rate of zoospore survival. From the models, it is clear that life-history trade-offs allow B. dendrobatidis to maintain a relatively high long-term growth rate at low temperatures, so that it maintains high fitness across a range of temperatures. When a seven-day cold shock is simulated, the outcome is intermediate between the two constant temperature regimes, and in culture, a sudden drop in temperature induces zoospore release. These trade-offs can be ecologically important for a variety of organisms with complex life histories, including pathogenic microorganisms. The effect of temperature on amphibian mortality will depend on the interaction between fungal growth and host immune function and will be modified by host ecology, behavior, and life history. These results demonstrate that B. dendrobatidis populations can grow at high rates across a broad range of environmental temperatures and help to explain why it is so successful in cold montane environments.     

Dynamics and management of infectious disease in colonizing populations

The introduction of chronic, infectious diseases by colonizing populations (invasive or reintroduced) is a serious hazard in conservation biology, threatening the original host and other spillover species. Most research on spatial invasion of diseases has pertained to established host populations, either at steady state or fluctuating through time. Within a colonizing population, however, the spread of disease may be influenced by the expansion process of the population itself. Here we explore the simultaneous expansion of a colonizing population and a chronic, nonlethal disease introduced with it, describing basic patterns in homogeneous and structured landscapes and discussing implications for disease management. We describe expected outcomes of such introductions for three qualitatively distinct cases, depending on the relative velocities at which the population and epidemic expand. (1) If transmissibility is low the disease cannot be sustained, although it may first expand its range somewhat around the point of introduction. (2) If transmissibility is moderate but the wave-front velocity for the population, vp, is higher than that for the disease, vd, the disease wave front lags behind that of the population. (3) A highly transmissible disease, with vd > vp, will invade sufficiently rapidly to track the spread of the host. To test these elementary theoretical predictions, we simulated disease outbreaks in a spatially structured host population occupying a real landscape. We used a spatially explicit, individual-based model of Persian fallow deer (Dama mesopotamica) reintroduced in northern Israel, considering a hypothetical introduction of bovine tuberculosis. Basic patterns of disease expansion in this realistic setting were similar to our conceptual predictions for homogeneous landscapes. Landscape heterogeneity, however, induced the establishment of population activity centers and disease foci within them, leading to jagged wave fronts and causing local variation in the relative velocities at which the population and epidemic expanded. Based on predictions from simple theory and simulations of managed outbreaks, we suggest that the relative velocities at which the population and epidemic expand have important implications for the impact of different management strategies. Recognizing which of our three general cases best describes a particular outbreak will aid in planning an efficient strategy to contain the disease.     

A test on social behavior as a cause of dispersal of spruce grouse

Summary Social behavior is one hypothesized cause for dispersal. We tested this hypothesis on spruce grouse (Dendragapus canadensis) in two years by removing adults in summer and monitoring emigration of juveniles in autumn. Despite the absence of adults, juveniles emigrated from the natal range at rates comparable to juveniles on control areas. Data on density and dispersal from earlier spruce grouse studies are reviewed, which show that emigration is constant despite substantial differences in density, and that a clear female sex bias occurs across a wide range of densities. Results do not support the hypothesis that social behavior influences dispersal nor do they support a prediction of the Oedipus hypothesis that no sex bias occurs in polygynous birds. Offprint requests to: D.M. Keppie     

Terrestrial runoff as a cause of outbreaks of Acanthaster planci (Echinodermata: Asteroidea)

Outbreaks of adult Acanthaster planci (Linnaeus) have appeared at irregular intervals, arriving 3 yr after heavy rains (>100 cm in 3 months) following droughts (<25 cm in 4 months) or 3 yr after rains exceeding intensities of 30 cm in 24 h. Outbreaks of A. planci follow typhoons that bring heavy rains, but do not follow dry typhoons of equivalent wind force. Outbreaks occur around the high islands in Micronesia and Polynesia, but not around the atolls at intermediate locations. Phytoplankton blooms appear off high islands at the beginning of the rainy season in bays with large watersheds and with sufficient residence time of the waters; these are the initial sites of A. planci abundance on Guam. The spawning seasons of A. planci occur at the beginning of the rainy season on both sides of the equator. I hypothesize that, on rare occasions, terrestrial runoff from heavy rains (following the dry season or a record drought) may provide enough nutrients to stimulate phytoplankton blooms of sufficient size to produce enough food for the larvae of A. planci. The increased survival of larvae results in an outbreak of adults 3 yr later. This hypothesis can be tested by predicting future outbreaks. An outbreak of A. planci on Saipan in the summer of 1981 was predicted on the basis of heavy rains in August 1978.Contribution no. 169, University of Guam Marine Laboratory     

Life history benefits of residency in a partially migrating pond-breeding amphibian

Species with partial migration, where a portion of a population migrates and the other remains residential, provide the opportunity to evaluate conditions for migration and test mechanisms influencing migratory decisions. We conducted a five-year study of two populations of red-spotted newts (Notophthalmus viridescens), composed of individuals that either remain as residents in the breeding pond over the winter or migrate to the terrestrial habitat. We used multistate mark-recapture methods to (1) test for differences in survival probability between migrants and residents, (2) determine if migrants breed every year or skip opportunities for reproduction, and (3) estimate the frequency of individuals switching migratory tactic. We used estimates of life history parameters from the natural populations in combination with previous experimental work to evaluate processes maintaining partial migration at the population level and to assess mechanisms influencing the decision to migrate. Based on capture-recapture information on over 3000 individuals, we found that newts can switch migratory tactics over their lifetime. We conclude that migrants and residents coexist through conditional asymmetries, with residents having higher fitness and inferior individuals adopting the migrant tactic. We found that newts are more likely to switch from residency to migrating than the reverse and males were more likely to remain as residents. Migration differences between the sexes are likely driven by reproduction benefits of residency for males and high energetic costs of breeding resulting in lower breeding frequencies for females. Environmental conditions also influence partial migration within a population; we found support for density-dependent processes in the pond strongly influencing the probability of migrating. Our work illustrates how migration can be influenced by a complex range of individual and environmental factors and enhances our understanding of the conditions necessary for the evolution and maintenance of partial migration within populations.     

Spatial spread of an emerging infectious disease: conjunctivitis in House Finches

In this paper we quantify the rate of spread of the newly emerged pathogen Mycoplasma gallisepticum of the House Finch, Carpodacus mexicanus, in its introduced range. We compare and contrast the rapid, yet decelerating, rate of spread of the pathogen with the slower, yet accelerating rate of spread of the introduced host. Comparing the rate of spread of this pathogen to pathogens in terrestrial mammalian hosts, we see that elevation and factors relating to host abundance restrict disease spread, rather than finding any major effects of discrete barriers or anthropogenic movement. We examine the role of seasonality in the rate of spread, finding that the rate and direction of disease spread relates more to seasonality in host movement than to seasonality in disease prevalence. We conclude that asymptomatic carriers are major transmitters of Mycoplasma gallisepticum into novel locations, a finding which may also be true for many other diseases, such as West Nile Virus and avian influenza.     

Metabolic rates of epipelagic marine copepods as a function of body mass and temperature

Metabolic rates (oxygen consumption, ammonia excretion, phosphate excretion) have been calculated as a function of body mass (dry, carbon, nitrogen and phosphorus weights) and habitat temperature, using multiple regression. The metabolic data used for this analysis were species structured, collected from Arctic to Antarctic seas (temperature range: -1.7°C to 29.0°C). The data were further divided into geographical and/or seasonal groups (35 species and 43 data sets for oxygen consumption; 38 species and 58 data sets for ammonia excretion; 22 species and 31 data sets for phosphate excretion). The results revealed that the variance attributed to body mass and temperature was highest (93-96%) for oxygen consumption rates, followed by ammonia excretion rates (74-80%) and phosphate excretion rates (46-56%). Among the various body mass units, the best correlation was provided by the nitrogen unit, followed by the dry weight unit. The calculated Q₁₀ values varied slightly according to the choice of body mass units; overall ranges were 1.8-2.1 for oxygen consumption rates, 1.8-2.0 for ammonia excretion rates and 1.6-1.9 for phosphate excretion rates. The effects of body mass and temperature on the metabolic quotients (O:N, N:P, O:P) were insignificant in most cases. Although the copepod metabolic data used in the present analysis were for adult and pre-adult stages, possible applications of the resultant regression equations to predict the metabolic rates of naupliar and early copepodite stages are discussed. Finally, global patterns of net growth efficiency [growth (growth+metabolism)^-1] of copepods were deduced by combining the present metabolic equation with Hirst and Lampitt's global growth equation for epipelagic marine copepods.     

Setting population targets for mammals using body mass as a predictor of population persistence

Conservation planning and biodiversity assessments need quantitative targets to optimize planning options and assess the adequacy of current species protection. However, targets aiming at persistence require population‐specific data, which limit their use in favor of fixed and nonspecific targets, likely leading to unequal distribution of conservation efforts among species. We devised a method to derive equitable population targets; that is, quantitative targets of population size that ensure equal probabilities of persistence across a set of species and that can be easily inferred from species‐specific traits. In our method, we used models of population dynamics across a range of life‐history traits related to species’ body mass to estimate minimum viable population targets. We applied our method to a range of body masses of mammals, from 2 g to 3825 kg. The minimum viable population targets decreased asymptotically with increasing body mass and were on the same order of magnitude as minimum viable population estimates from species‐ and context‐specific studies. Our approach provides a compromise between pragmatic, nonspecific population targets and detailed context‐specific estimates of population viability for which only limited data are available. It enables a first estimation of species‐specific population targets based on a readily available trait and thus allows setting equitable targets for population persistence in large‐scale and multispecies conservation assessments and planning.     

Population dynamics of Diadema antillarum (Echinodermata: Echinoidea) following mass mortality in Panamá

In 1983, Diadema antillarum suffered mass mortality throughout the Caribbean Sea and the western Atlantic Ocean. I followed the dynamics of populations at the San Blas Islands, Panamá from April 1983 to November 1987. Density measurements indicate that populations of D. antillarum have not recovered from the die-offs that killed nearly 97% of the individuals. There was recruitment to the 1 to 1.5 cm class immediately after the mass mortality, but there has been little additional influx of juveniles since then. The low number of observable juveniles could not be attributed to elevated rates of predation on very small individuals. Rates of recruitment did not differ between reefs with artificially increased densities of D. antillarum and reefs kept free of sea urchins; thus, the lack of recruitment did not arise from absence of adults that could provide settlement cues to the larvae or protection to newly settled juveniles. Other species of sea urchins did not show a clear pattern of increase after the demise of D. antillarum. Therefore, interspecific competition directed towards D. antillarum juveniles did not increase after the mass mortality. Two reefs where Echinometra viridis, Eucidaris tribuloides and Lytechinus williamsi, were removed showed no significant differences in recruitment of D. antillarum relative to two reefs where these species were allowed to remain at their natural densities. Resident D. antillarum after the mass mortality produced gametes with the same per capita intensity and lunar synchrony as before the mass mortality. However, it is possible that the probability of fertilization of their gametes decreased because of low population density. The most likely explanation for lack of recruitment is that the reduced numbers of reproducing adults at Panamá and upstream locations resulted in levels of larval supply that were inadequate to sustain recruitment on Panamanian reefs.     

How identity of the homopteran trophobiont affects sex allocation in a symbiotic plant-ant: the proximate role of food

We provide evidence for the proximate role of food in sex allocation by an ant species, and demonstrate how identity of the homopteran partner affects benefits to colonies of a plant-symbiotic ant. The system studied includes a plant-ant that nests in swollen hollowed internodes of a myrmecophyte, and two species of homopteran trophobionts (a coccid and a pseudococcid) tended inside domatia by these ants, for which they are an essential source of food. Total investment in pupae was greater for ant colonies that tended solely or primarily coccids than for those that tended pseudococcids. In particular, biomass invested in sexuals increased more rapidly with size of the colony in trees where ants tended coccids. This greater investment in sexuals was not made at the expense of investment in workers, but reflected increased resources available to coccid-tending colonies. Higher reproductive output indicates that ant fitness may be greater when they tend coccids. These additional resources led to a greater increase in production of alate females than in that of males. Consequently, the sex investment ratio of coccid-tending colonies was more female biased than in those that tended pseudococcids. Differences in resource supply affected numbers of individuals produced but not per-individual investment, with one partial exception: in very small colonies, pseudococcid-tending colonies produced small workers while coccid-tending colonies did not, further underlining the higher resource supply to coccid-tending colonies. This study provides evidence for the proximate role played by food in sex allocation at the colony level. We discuss our results in the context of hypotheses aimed at explaining sex ratio at the colony and population levels.     

Increases in surgeonfish populations after mass mortality of the sea urchinDiadema antillarum in Panamá indicate food limitation

In 1983/1984,Diadema antillarum suffered mass mortalities throughout its West Atlantic range. Its populations were reduced by 95% and subsequently have failed to recover. These die-offs led to sustained increases in the abundance of soft algae, including types eaten by herbivorous reef fishes. I monitored adult populations of three herbivorous surgeonfishes (Acanthurus coeruleus, A. chirurugus andA. bahianus) between 1978 and 1990, and the recruitment of their pelagic juveniles between 1979 and 1989, on six patch reefs in Panamá. Adult populations ofA. coeruleus andA. chirurgus, which largely restrict their feeding to reef substrata, increased by averages of 250 and 160%, respectively, after the die-off ofD. antillarum in 1983. No increases occurred in the adult populations ofA. bahianus, which often feeds in off-reef habitats unaffected byD. antillarum. Average annual levels of juvenile recruitment of all three surgeonfishes did not differ before and after the die-off. These results support the hypothesis that adult populations of two herbivorous fishes that are strongly reliant on reef algae for food previously were limited by competition withD. antillarum.     

Utilization of a fecal mass as food by the pelagic mysis larva of the penaeid shrimp Solenocera atlantidis

The undetached peritrophic membrane of the mysis shrimp larva (Solenocera atlantidis) provides a substratum on which microbes, organic debris and planktonic organisms accumulate. Behavioral, metabolic and biochemical data indicate that this fecal mass serves as a concentrated food resource for the larva.     

Genital abnormalities in white-tailed deer (Odocoileus virginianus) in west-central Montana: pesticide exposure as a possible cause

From spring, 1996, to early spring, 2000, accident-killed and injured white-tailed deer, Odocoileus virginianus, in the Bitterroot Valley of west-central, Montana, U.S.A., were collected and examined for genital abnormalities at the Bitterroot Wildlife Rehabilitation Center. Of the 254 male deer examined, 133 were fawns aged 3 months to 1 yr, 29 were 1 to 1 1/2 yrs of age, and 92 were 1 1/2 to 3 yrs of age. Approximately 33% were normal; the remaining 67% showed varying degrees of apparent genital developmental anomalies, specifically mispositioned and undersized scrota and ectopic testes, and this percentage held through all age groups. The sex ratio of fawns and fetuses was skewed towards males, significantly so for the 1996 fawn cohort and for the total of all fawns and fetuses in the study. Although possible causes of the genital anomalies, centering on endocrine disrupting pesticides, are discussed, no conclusions of cause and effect can be currently justified.