An experimental study on the effects of an introduced parasite in Darwin’s finches

It is widely recognised that the main threats to the biota of the Galápagos Islands stem from newly introduced diseases, plants and animals. Introduced organisms may lead to the rapid extinction of naïve insular populations. Previous research on Galápagos showed that the parasitic larvae of the fly Philornis downsi occurred in virtually all nests of land bird species examined, with high nestling mortality (27% of all broods) in relation to high parasite infestation. In this study, we used an experimental approach to measure the fitness impacts of the fly larvae in two species of Darwin’s finch (Geospizinae). We created parasite-reduced nests by applying a 1% pyrethrin solution to the nest during the early nesting phase, and measured: (1) nestling growth, (2) nestling haemoglobin (Hb) concentration and (3) fledging success. A single insecticide treatment was sufficient to reduce parasite intensity to nearly zero, and revealed reduced mass gain and reduced fledging success in parasitized nests compared to parasite-reduced nests. This is the first experimental study of fitness impacts by Philornis on its host species. The results are discussed in the light of short-term protection measures for nests of rare finch species in the Galápagos archipelago.     

Parasite infection rates of impala (Aepyceros melampus) in fenced game reserves in relation to reserve characteristics

Under certain conditions reserves can pose a threat to wildlife conservation by increasing the transmission of parasites and pathogens. In this study, I investigated associations between reserve characteristics including area, density and species richness and parasite infection rates in impala (Aepyceros melampus). Using coprological methods to measure gastrointestinal parasitism rates of impala inhabiting five fully or partially fenced game reserves in central Kenya, I found that bovid species richness was correlated with parasite taxa richness across reserves, and that prevalence rates of multi-host strongyle nematodes were higher in reserves with more species. In addition, reserve size was also implicated as a potential predictor of infection risk. Overall, these results suggest that wildlife inhabiting highly diverse and small reserves may suffer from higher than normal rates of infection. Given the potential debilitating effects increases in parasitism can have on wildlife, these results underscore the importance of considering parasite transmission dynamics in the management of small, fenced protected areas.     

Increasing nest success in the yellow-shouldered blackbird Agelaius xanthomus in southwest Puerto Rico

The yellow-shouldered blackbird, Agelaius xanthomus, is endemic to Puerto Rico and Mona Island, and endangered since 1976 mainly because of brood parasitism by the shiny cowbird, Molothrus bonariensis. In 1984 an artificial nest structures program was initiated, combined with the removal of M. bonariensis, to improve the reproductive success of A. xanthomus. The nesting success was high in artificial nest structures. From 1996 to 1999, 22 out of 804 nests in artificial structures and one of 203 nests in natural substrates were parasitized. The use of natural substrates increased from less than 1% (1996) to 35% (1999). Predation was the main cause of egg and chick loss and was high in natural substrates. The increase in the use of natural substrates for nesting is a trend favorable for the recovery of this species. Continued management is still needed to augment the breeding population and reproductive output.     

An analysis of the role of local fishermen in the conservation of the loggerhead turtle (Caretta caretta) in Pontal do Ipiranga, Linhares, ES, Brazil

The role of researchers and fishermen in the clutch management of loggerhead sea turtles was evaluated for 10 nesting seasons at Pontal do Ipiranga TAMAR station, Linhares, ES. The comparison of nests transferred by researchers and locals (carebeiros) showed that clutches transferred by researchers presented higher clutch size. Clutch size between nests transferred by carebeiros and left in situ did not show significant differences. Hatching success was significantly higher for clutches left in situ than for those transferred to other places in the beach or to hatcheries. The clutches transferred exclusively by researchers achieved a higher hatching success than those transferred partially or totally by carebeiros. The relocation time of clutches collected by carebeiros and handed to researchers affected hatching success. It is recommended that clutches be left in situ, provided they have adequate conditions for monitoring, but careful clutch translocation, independent of the interval elapsed after laying, may also constitute a viable technique for the conservation of sea turtles in the region.     

Plasmodium blood parasite found in endangered Galapagos penguins (Spheniscus mendiculus)

This is the first report of a Plasmodium blood parasite found in the Galapagos Archipelago. Phylogenetic analyses place this parasite, recovered from endangered Galapagos penguins (Spheniscus mendiculus), within the genus Plasmodium, and suggest a close relationship to some of the most dangerous lineages of Plasmodium that have been known to cause severe mortality and morbidity in captive penguin populations. Infectious disease is an increasingly important cause of global species extinctions, and extinctions due to avian pox and avian malaria (Plasmodium relictum) have been well documented in Hawaiian avifauna. Plasmodium blood parasites had not been detected in Galapagos birds until now, despite previous microscopic and molecular screening of many of the species, including the Galapagos penguin. While penguin populations now appear healthy, it is unclear whether this parasite will have an obvious impact on their survival and reproduction, particularly during El Niño events, which cause stress due to reduced food availability. It is possible that this parasite arrived with or shortly after the recent arrival of an introduced mosquito, Culex quinquefasciatus, known elsewhere as a competent vector of Plasmodium blood parasites.     

Hyperparasitism of oospores of Phytophthora megasperma var. sojae

Hyperparasites of oospores of Phytophthora megasperma Drechs. var. sojae Hildb. were present in each of 15 field soils tested. Maximum numbers of oospores parasitized ranged from 42.5 to 87.5% for flooded soils, and from 25.5 to 73.0% for soils adjusted to 50% water holding capacity; the mean for all soils was 51.5%. The frequency of hyperparasitism was not correlated with the disease potential soils for Phytophthora root-rot of soybean as determined in seedling tests on flooded soil samples. Of eight isolated hyperparasitic fungi tested in steamed soil, the most efficient parasites were Hyphochytrium catenoides, Humicola fuscoatra, and Pythium monospermum, each of which parasitized at least 76% of oospores during 3 weeks. Hyphae were not parasitized by any of the eight fungi. Parasitism by H. catenoides in sterilized soil increased as soil temperature increased from 16° to 28°C. Parasitism by P. monospermum was maximum at 20°–24°C. Oospores of P. meyasperma var. sojae race 7 were more resistant to infection by hyperparasites than were oospores of races 1 and 3. Oospores produced in culture were slightly more susceptible to hyperparasitism in soils than were oospores produced in soybean seedlings.     

Exposure to ecotourism reduces survival and affects stress response in hoatzin chicks (Opisthocomus hoazin)

Ecotourism helps to protect many habitats, but may also have negative impacts on wildlife. We investigated effects of ecotourists on reproductive success of hoatzins (Opisthocomus hoazin) and on hormonal status of their chicks in Amazonian rainforest lakes by comparing birds from undisturbed and from tourist-exposed nests. Hatching success was similar in both groups but chick survival was much lower at tourist-exposed nests than at undisturbed nests. This effect was due to an increased mortality of juveniles prior to fledging whereas small nestlings seemed largely unaffected. Juveniles, but not nestlings, living at tourist-exposed sites had a lower body mass and showed a stronger hormonal response to experimental stress compared to individuals at undisturbed sites. These data suggest that juvenile hoatzins were susceptible to tourist-induced stress which in turn may be responsible for the lower survival. In contrast, adult hoatzins that were incubating had apparently habituated to tourist presence because their flush distances at tourist-exposed nests were 50% lower than at undisturbed sites. Our findings demonstrate that individuals in different life stages show different susceptibilities to tourism. We suggest that even just watching animals during breeding can threaten their survival, but a proper scientific management of off-limit zones and area-specific guidelines for wildlife observation could reduce harmful effects.     

Holoparasitic Cuscuta campestris suppresses invasive Mikania micrantha and contributes to native community recovery

Traditional biocontrol uses introduced non-native agents to control alien invasive species. Recently, using species of the invaded regions to control invaders has been proposed as a potential alternative to traditional biocontrol. To explore the effects of the obligate parasite Cuscuta campestris in the invaded regions on controlling the alien invasive weed Mikania micrantha and on recovering the heavily invaded communities in the coastal Guangdong Province in South China, we conducted a field survey in four sites on the Neilingding Island where Cuscuta has been artificially introduced to the Mikania-invaded communities for one to 4 years, and also three sites in Shenzhen, Dongguan and Haifeng where the Mikania-invaded communities have been naturally parasitized by Cuscuta for at least 5 years. Cuscuta effectively suppressed the growth and invasiveness of Mikania, leading to its decline. The restraint on Mikania by Cuscuta increased richness and diversity of native plants, contributing to native community recovery. Moreover, Cuscuta declined with decreasing Mikania, and its parasitism rate on Mikania was much higher than that on the native species, suggesting little non-target effects. The effects of Cuscuta varied little among sites of Shenzhen, Dongguan and Haifeng, but increased greatly with time of introduction on the Neilingding Island. Our results suggest that Cuscuta is an effective agent for controlling Mikania, and that enemies of the invaded regions may be a promising alternative to traditional biocontrol.     

High genetic diversity and heterogeneous parasite load in the earthworm Lumbricus terrestris on a German meadow

In parasite-host dynamics, parasites exert frequency-dependent selection on their hosts by favouring rare alleles that may confer resistance against infection. Therefore host populations that suffer strong parasite stress should maintain higher levels of genetic variability. We studied the Lumbricus terrestris-Monocystis sp. host-parasite system at a microgeographical scale. Using three polymorphic microsatellite loci on one large earthworm population sampled at 26 different sites (281 genotypes), we tested the relationship between parasite load and genetic variation in natural samples of the common earthworm L. terrestris. Our analysis yielded the following: (1) parasite load varied significantly across sites in this population; (2) there was no consistent evidence for heterozygote deficiency (observed heterozygosities ranged between 0.74 and 0.87), indicating a low level of inbreeding; (3) there was no significant genetic structuring among sample sites; (4) we could not identify a significant association between parasite load and population genetic diversity; (5) there was considerable population differentiation (15.17%) between our German samples and a Canadian L. terrestris reference population. Our study provides insight into the population genetics of one of the most economically important soil organisms on a microgeographic scale.     

Human land use and patterns of parasitism in tropical amphibian hosts

Landscape alterations by humans can change patterns of parasite transmission. Depending on the type alteration and the life histories of parasites and hosts, parasitism may increase or decrease. To investigate whether parasitism in tropical amphibians was associated with land use change, I studied three species of amphibians, Rana vaillanti, Eleutherodactylus fitzingeri, and Smilisca puma from the Province of Heredia, Costa Rica, in the Atlantic lowlands. Frogs were collected and examined for parasites during the rainy seasons of 2001-2003 from sites in forest or clear-cut cattle pastures. The abundances of five species of parasites and parasite species richness of R. vaillanti were significantly higher in pasture habitat. A single parasite species shared by E. fitzingeri and S. puma showed a trend of increased abundance in pasture habitats. Overall, the abundances of six parasite species (three trematodes, an intestinal nematode, an encysted nematode, and a filarial nematode) were higher in pastures, while two species (trematodes) were higher in forest. This study suggests that land use activities in tropical regions affects the abundance and richness of amphibian parasites. Converting forest to pasture may impact the abundance of amphibian parasites because subsequent water quality changes (e.g. eutrophication, higher pH) often enhance habitat and resources for intermediate hosts (e.g. snails, mosquitoes) involved in parasite life cycles. Aquatic amphibians (e.g. R. vaillanti) may be particularly prone to experiencing increases in parasitism in agricultural habitats due to the positive relationship between many aquatic intermediate hosts and water quality changes associated with agricultural land use.     

Association of wetland acidity with reproductive parameters and insect prey of the Eastern Kingbird (Tyrannus tyrannus) near Sudbury,Ontario

A three year study (1981 to 1983) was conducted to determine possible influences of wetland acidification on the reproduction and growth of the Eastern Kingbird (Tyrannus tyrannus). This species uses emergent aquatic insect prey to feed its nestlings. Egg characteristics and nestling growth were monitored for birds nesting in 26 lakes in the Killarney region near Sudbury, Ontario (pH range 4.27 to 6.26). The major percentage of variation in kingbird reproductive factors including clutch initiation, egg weight loss and torso-metatarsus bone growth was explained by differences between siblings and among nests on a single lake. A smaller percentage of the variance in reproductive parameters was explained by the variation in water chemistry among lakes. Canonical correlation showed that sulfate, nitrate/nitrite, alkalinity, pH, and several metals (Fe, Mn, Al) accounted for a minor but significant variance in growth characteristics. These water chemistry parameters are influenced by lake acidification. The relationship observed between lake acidity and kingbird reproduction is therefore measurable but minor compared to the influence of genetic and inter-nest variables. The study showed no food limitation for the kingbird attributed to lake acidity.     

Does the acephaline gregarine Monocystis sp. modify the surface behaviour of its earthworm host Lumbricus terrestris?

The earthworm Lumbricus terrestris has relatively low dispersal rates. This can represent a challenge for the internal gregarine parasite Monocystis, the dispersal of which often depends on the host. Mating of Monocystis can also be restricted to parasite stages within the current host individual. Adaptations, including host behavioural modification, that improve parasite transmission and simultaneously avoid inbreeding within a single host individual should be favoured by selection. We used a correlative approach to investigate the question of parasitic manipulation in this Gregarine-Lumbricid system. We observed mature earthworms (n=24) for 3 weeks while recording various measures of activity (surface activity, burrowing activity, surfacing delay, number of surface visits) and correlated parasite load with these activity measures. We found a significant positive correlation between surface activity and midden (or cast) production, which suggests a simple method for assessing the overall activity of local earthworm populations. However, we found no evidence of behavioural manipulation of any measure of host activity. We discuss these results in the context of inbreeding depression and host-parasite coevolution.     

Differences in the reproductive success and survival of the rufous treecreeper (Climacteris rufa) between a fragmented and unfragmented landscape

The rufous treecreeper (Climacteris rufa) has declined in abundance in the agricultural regions of southwestern Australia. The patterns of decline are well documented, but the processes that threaten population persistence are poorly understood. I compared the reproductive success and survival of the treecreeper between three sites in an unfragmented landscape and four remnant categories (large, small, grazed and ungrazed) in a fragmented, agricultural landscape. Nest success and annual productivity were significantly higher in the unfragmented landscape, but varied between sites and remnant categories within landscapes. Nest success was lowest in grazed remnants and annual productivity was positively associated with territory size in the fragmented landscape. Fledgling survival rates did not differ between landscapes, but there was a trend for juvenile survival rates to be higher in the unfragmented landscape. I used artificial nests to compare relative predation rates between landscapes, and provisioning rates and prey biomass brought to nestlings to assess differences in food availability. There were no landscape differences in predation rates, but provisioning rates to nestlings and total prey biomass were significantly lower in the fragmented landscape. Mean habitat quality was also lower in the fragmented landscape, although it differed between remnant categories. Reduced reproductive success, juvenile survival, food availability and habitat quality may threaten the viability of the rufous treecreeper population living in the fragmented landscape. Limiting the modification of remaining habitat (e.g. removing stock grazing) and improving habitat quality are required to assist in the conservation of this species.     

Introduced cane toads Bufo marinus are active nest predators and competitors of rainbow bee-eaters Merops ornatus: observational and experimental evidence

During a three-year study, introduced cane toads (Bufo marinus) ruined one-third of nest attempts of ground-nesting rainbow bee-eaters (Merops ornatus) by usurping their nest burrows and preying upon their eggs and young nestlings. Birds that had lost their nest to cane toads were less likely to be recaptured in subsequent years. Cane toads are having a significant negative effect at the population level: at present, rainbow bee-eaters produce 0.8 fledglings per nest. However, in the absence of cane toads each nest would produce 1.2 fledglings. Rainbow bee-eaters had little defence against the cane toads. The diurnal birds were not able to mob the nocturnal toads, nor were they able to eject cane toads from the nest. Deep nests and nests built on steep slopes were still preyed upon by the toads. Cane toads that were removed from the nest had the ability and motivation to return to the nest when displaced up to 1200 m away, suggesting that the nest is a valuable resource to toads. Cane toads were significantly more likely to: (a) prey upon nests containing hatchlings rather than eggs; (b) enter and occupy artificial nest tunnels (1.2 m deep) containing a small food item (20 g of raw chicken) rather than artificial nests that were empty. These results indicate that cane toads actively prey upon nests using olfactory cues. The predatory and homing abilities of cane toads are reviewed, as well as their need for diurnal shelter sites. The possibility that cane toads are having a negative impact upon other native, ground-dwelling vertebrate fauna via their role as opportunistic predators requires urgent investigation.     

Optimal release strategies for captive-bred animals in reintroduction programs: Experimental infections using the guppy as a model organism

Reintroduction of captive-bred individuals for supplementation or re-establishment of wild populations has become increasingly important to prevent the extinction of many endangered species. Despite the importance of reintroductions for conservation biology, few studies have empirically evaluated the potential impacts of reintroductions of naïve organisms on disease outbreaks in native wild populations. Here, we use a model organism, the guppy (Poecilia reticulata) and its ubiquitous parasite (Gyrodactylus turnbulli) to evaluate: (i) the most effective release procedure (i.e. en masse vs. gradual release) that minimises host mortality and parasite load, (ii) the effect of pre-exposure to the parasite on host susceptibility, and (iii) the potential advantage of removing the most susceptible individuals before release. We could not detect a statistically significant difference in host survival rates between release protocols and pre-exposure regime. However, the parasite population went extinct significantly more often when pre-exposed fish were released. Furthermore, the parasite load of individual guppies by the end of the reintroduction was significantly lower in treatments where fish had been pre-exposed to parasites than in treatments with naïve guppies. Additionally, pre-exposure of hosts provided important information about their level of resistance when reintroduced. These findings suggest that pre-exposure to native parasites could be beneficial for the survival rate of captive-bred animals when reintroduced in the wild. We discuss the practicalities of these potential release strategies.     

Effects of agricultural landscape and pesticides on parasitism in native bullfrogs

Native amphibian populations are shrinking worldwide, and both parasitic infections and environmental stress from agriculture have been implicated. We investigated the principal hypothesis that environmental by-products of agricultural activity mediate parasitism in native frogs. Bullfrogs were collected from wetlands with variable landscape disturbance and water quality and examined for helminth parasites. We predicted that pesticide pollution and landscape development would be significant factors shaping the parasite communities and populations. Parasite diversity and species richness were lower in wetlands impacted by both pesticides and land use. Two parasite groups, direct life-cycle nematodes and echinostomes, were common in polluted habitats, potentially increasing frog pathology and mortality risk. In areas with agricultural landscape and reduced forest cover, parasite diversity and species richness were low, perhaps because of less parasite transmission from birds and mammals. This result suggests that land development limits terrestrial vertebrate access to wetlands. Our results indicate that parasite abundance and community structure in wetlands are influenced by factors operating locally within the wetland and more broadly in the surrounding landscape. We suggest that parasite communities in amphibians are effective indicators of ecosystem health and animal biodiversity, and thus useful tools for conservation biology.     

Adapting to changing poaching intensity of yellow-shouldered parrot (Amazona barbadensis) nestlings in Margarita Island, Venezuela

The yellow-shouldered parrot (Amazona barbadensis) is listed in Venezuela as Endangered and internationally as Vulnerable, primarily due to poaching for the illegal pet trade. Various interventions have been implemented to reduce poaching (increasing the population from 700 in 1989 to 1600 in 2009), but poaching pressure is still high, and is ever-changing, requiring an evolving response. Between 2000 and 2003, our only intervention was environmental education in schools: in the short term, unsurprisingly, it had no impact on poaching, which reached 100% of nestlings in monitored nests. From 2004 onwards, we implemented a set of new field interventions. In 2004, 24 h field surveillance decreased poaching to 56%. In 2005, the addition of foster nests and a pilot test of “assisted breeding” brought the figure down to 18%. In 2006, assisted breeding was expanded, achieving 0% poaching. In 2007, poachers raided our “secure” site, and took 34 nestlings, bringing poaching up to 60%. A pilot study of artificial nests offered promising results. In 2008 and 2009, the addition of patrolling by local police reduced poaching to 16% and 1%, respectively. During 2004–2009, nestling poaching averaged 25%. Ensuring parrot recruitment in the future will require a combination of the strategies employed to date; in the short term, expanding the use of artificial nests to increase availability of nesting sites in easily-patrolled areas has the most potential to build on past successes.     

Regulation of parasitism by host density: The Bdellovibrio-Rhizobium interrelationship

Rhizobium strains of the cowpea group did not lose viability readily when added to soil, but Bdellovibrio acting on these rhizobia were found in 32 of 90 soils examined. Bdellovibrio did not initiate replication in liquid media at low host densities, but it did multiply once the Rhizohium numbers increased through growth to about 10⁸ ml^?1. From about 10⁴ to 6 × 10⁵ ml^?1Rhizohium cells survived attack by the parasites in liquid media. In nutrient-free buffer, no significant increase in vibrio abundance was evident if the rhizobial frequency was low. whereas Rhizobium populations containing 6 × 10⁸ cells ml^?1 were lysed rapidly. Bdellovibrio did not multiply when introduced into sterile soil with small numbers of the host, but it replicated when the rhizobia were abundant because of the latter's use of soil organic matter for growth or because of the deliberate addition of 10⁸Rhizohium g^?1. Nevertheless, the host persisted in such vibrio-rich soil samples. The abundance of indigenous bdellovibrios increased appreciably in nonsterile soil if the rhizobia were introduced in large but not small numbers. It is suggested that a major reason for the lack of elimination of the host population in soil by its parasites is the need for a critical host cell frequency, large Rhizobium numbers being required for Btiellovibrio to initiate replication and low numbers of surviving hosts no longer being able to support the parasite.     

Impact of introduced birds on the recovery of the Tahiti Flycatcher (Pomarea nigra), a critically endangered forest bird of Tahiti

In 1998, only 25 Tahiti Flycatchers (Pomarea nigra), a forest bird endemic to Tahiti (French Polynesia) remained. A recovery programme, aimed at nest protection through both rodent control and tree banding, was initiated. At this time it was supposed that the species was mainly the victim of island infestation by ship rats (Rattus rattus). In the 3 years of this study 54 nests were found and 17 fledged young produced, of which 12 survived the early stage of fledging. Despite an excellent 1999 breeding season and efficient nest protection against rodents, only five of 19 nests produced fledged young in 2000. This was related to higher (P=0.002 and 0.015 respectively) Indian Mynah (Acridotheres tristis) encounters and aggressive interactions in 2000 and 1998 than in 1999. Indian Mynah encounters and interactions were also higher during reproductive activities (and particularly at incubation and nestling stages) in comparison with the non breeding period (P <0.001). In contrast, Red-vented Bulbul (Pycnonotus cafer) encounters and interactions were more uniform throughout. Significantly more Indian Mynah and Red-vented Bulbul were observed in flycatcher territories which experienced nest failure or early fledgling death in comparison with those which experienced reproductive success (P=0.003 and 0.002 respectively). This strongly suggests that these two introduced species represent an important threat to the Tahiti Flycatcher’s survival. Currently, young birds (less than 4 years old) represent 42% of the population, an increase from 12% at the start of the recovery programme.     

Impact of grassland farming intensification on the breeding ecology of an indicator insectivorous passerine, the Whinchat Saxicola rubetra: Lessons for overall Alpine meadowland management

The decline of insectivorous farmland passerines has been attributed mostly to global decrease in arthropod availability, as a result of intensification of agricultural practices. The diminution of the Alpine Whinchat, once a widespread insectivorous passerine, has been ascribed to nest losses due to earlier and more frequent mowings. However, potential conjugated effects of deteriorated arthropod food availability had yet to be investigated. We compared food supply and nestling diet in intensively vs. traditionally managed grassland. Abundance and diversity of arthropods were much lower in intensive areas, where small-sized invertebrates, which do not enter nestling diet, were also predominant. Parents breeding in intensive habitats fed less biomass to nestlings than adults from traditional habitats. Nestling diet was less diverse and dominated by less profitable prey items in intensive than in traditional habitats. Feeding rate did not differ between the two habitats, but foraging distances from nest tended to be greater in intensive farmland. There were no significant differences in clutch sizes and hatching success with respect to management intensity, but fledging success was higher in traditional habitats. The recent intensification of farming practices has led to a decrease in the availability of grassland invertebrates, and of important Whinchat nestling food in particular, affecting parents’ foraging efficiency and reproductive success. Conservation actions must not only reduce nest losses by postponing mowing, but should also promote grassland farming that is less detrimental to invertebrates. Dominant at the study site, organic grassland farming does seemingly not provide sufficient conditions for Alpine Whinchats.