Successional mosquito dynamics in surrogate treehole and ground-container habitats in the northeastern United States: where does Aedes albopictus fit in?

This study assessed the risk of larval displacement of the eastern treehole mosquito, Aedes triseriatus, and the northern house mosquito, Culex pipiens, by Aedes albopictus, the Asian tiger mosquito, during the establishment and successional stages of novel larval mosquito treehole and ground-container habitats in the state of New Jersey, U.S.A. Culex pipiens and Culex restuans were the first mosquito species to colonize ground-container habitats and were the dominant larval species throughout the study period, whereas Ae. albopictus was late to colonize ground habitats and accounted for less than 15% of weekly larval collections once established. Ae. albopictus had a much stronger community presence within treehole ovitraps; however, Ae. albopictus never reached the average larval densities of the expected primary colonizer, Ae. triseriatus. Throughout the study period, the weekly abundances of Ae. triseriatus and Ae. albopictus were positively correlated and there were no significant differences between the abundances of each species. The larval dominance of Ae. triseriatus appears to be enhanced by the presence of Toxorhynchites rutilus septentrionalis, a large predatory mosquito species. When Tx. rut. septentrionalis was present, mature larvae (3(rd) -4(th) instar) of Ae. albopictus were also present in only 16.7% of collections, whereas mature larvae of Ae. triseriatus were collected concurrently with Tx. rut. septentrionalis in 53.8% of collections. These data suggest that Ae. triseriatus is at a greater risk of displacement by Ae. albopictus than are Cx. pipiens and Cx. restuans.

Drought-induced amplification of local and regional West Nile virus infection rates in New Jersey.

ABSTRACT This study looked at the influence of interannual variations in temperature and precipitation on seasonal mosquito abundances, the prevalence of West Nile virus (family Flaviviridae, genus Flavivirus, WNV) in the northeastern United States, and the capacity for local mosquito communities to maintain and transmit WNV, defined as vector community competence. Vector and virus surveillance took place within Middlesex County in New Jersey over two transmission seasons (2010 and 2011). Drought conditions during the 2010 season were associated with significant increases in the number of blood-fed Culex spp. mosquitoes collected per week, and significant increases in vector community competence, or the ability of local vector communities to transmit WNV, when compared with the wetter and milder 2011 season. These increases were associated with significantly higher weekly WNV infection rates in Culex spp. (i.e., Culex pipiens L. and Culex restuans L.) during the 2010 drought season. On a larger scale, the positive influence of drought on the amplification of WNV was also confirmed at the state level where early seasonal (June-July) increases in temperature and decreases in precipitation were strongly correlated with increases in yearly WNV infection rates over a 9-yr period (2003-2011). These data suggest that there may be clear temperature and precipitation thresholds beyond which epidemic levels of WNV transmission occur.

Abiotic versus biotic hierarchies in the assembly of parasite populations.

The presence or absence of parasites within host populations is the result of a complex of factors, both biotic and abiotic. This study uses a non-parametric classification tree approach to evaluate the relative importance of key abiotic and biotic drivers controlling the presence/absence of parasites with complex life cycles in a sentinel, the common killifish Fundulus heteroclitus. Parasite communities were classified from 480 individuals representing 15 fish from 4 distinct marsh sites in each of 4 consecutive seasons between 2006 and 2007. Abiotic parameters were recorded at continuous water monitoring stations located at each of the 4 sites. Classification trees identified the presence of benthic invertebrate species (Gammarus sp. and Littorina sp.) as the most important variables in determining parasite presence: secondary splitters were dominated by abiotic variables including conductance, pH and temperature. Seventy percent of hosts were successfully classified into the correct category (infected/uninfected) based on only these criteria. The presence of competent definitive hosts was not considered to be an important explanatory variable. These data suggest that the most important determinant of the presence of these parasite populations in the common killifish is the availability of diverse communities of benthic invertebrates.

Composition and diversity patterns in metazoan parasite communities and anthropogenic disturbance in stream ecosystems.

The composition and diversity of metazoan parasite communities in naturally depauperate ecosystems are rarely studied. This study describes the composition of helminth endoparasite communities infecting fish that are part of naturally acidic stream ecosystems in the coastal-plains region of the State of New Jersey (USA) known as the Pinelands, and compares the diversity of parasites between six streams that differ in anthropogenic disturbance. A total of 514 fish were examined representing 6 species native but restricted to the Pinelands region, 5 species native and widespread throughout the region and State, and 6 species introduced to the Pinelands and State. Fish (prevalence: 78%) were infected with 18 helminth endoparasite species. In most streams, prevalence of infection, mean abundance, and total number of individuals for the 5 most common parasites were higher in pirate perch, a native fish species. The diversity of helminth endoparasite communities measured as species richness and Shannon index was higher in degraded streams, and especially in native or introduced fish at these sites. Parasite diversity was positively correlated with anthropogenic disturbance, which was measured by water pH, water conductance, and the proportion of agricultural and developed land surrounding streams. Helminth community composition included parasites intimately tied to trophic interactions in food webs, and disturbance to these ecosystems results in changes to these communities. Understanding structure and function of animal communities from these naturally depauperate ecosystems is important before continued anthropogenic changes result in the extirpation or extinction of their unique fauna.

Anhydrobiosis increases survival of trichostrongyle nematodes.

This study demonstrates that infective-stage larvae of 2 trichostrongyle ruminant gastrointestinal nematodes, Haemonchus contortus and Trichostrongylus colubriformis, can enter into anhydrobiotic states when completely desiccated. Larvae of control trichostrongyle species, Heligmosomoides polygyrus and Nippostrongylus brasiliensis, that infect mice were unable to survive desiccation or to enter into anhydrobiosis. Ruminant larvae were able to survive up to 7 desiccation/rehydration cycles, and, during anhydrobiosis, metabolic activity was decreased and survival of the larvae was prolonged both in the laboratory and in the field. Relative humidity had no effect on ruminant larval survival after anhydrobiosis compared with controls. Temperature had a significant effect, 85.8 +/- 2.3% of larvae in anhydrobiosis could survive low temperatures (0 C) that killed all control larvae. Metabolic activity, measured by changes in lipid content and CO2 respiration, was significantly lower in larvae that entered anhydrobiosis compared with controls (P < 0.05). In field experiments using open-meshed chambers under ambient environmental conditions, larvae in anhydrobiosis had significantly higher survival rates in the field compared with controls (P < 0.05) during summer and winter trials. These data suggest that anhydrobiosis in ruminant larvae promotes survival at freezing temperatures, decreases metabolic activity, and prolongs survival under natural field conditions.

Fixed behaviours and migration in parasitic flatworms.

This paper considers how fixed behaviours may play a role in post-larval migrations of Entobdella soleae. A general argument is that a shift away from the paradigm of orientation is required to elucidate the mechanisms that parasites use to navigate on the surface of their hosts. Some migrations may rely on fixed behaviours (genetically programmed stereotyped behaviours) that often evolve under predictable environmental conditions with reliable signals. In turbulent and stochastic free-living environments, homeostatic hosts present very predictable topological substrates and physico-chemical characteristics to their parasites. Over the course of evolution on these predictable host substrates, adaptive behaviours in the parasites can become fixed. Examples of endoparasite migration behaviour, particularly that of the common liver fluke, Fasciola hepatica, will be used to develop an approach based on the perceptual worlds of migrating parasites. An important conclusion is that multi-disciplinary approaches, firmly rooted in an understanding of each parasite's natural history, are requisite to successful interpretation of migration behaviours on the host.

Estimating transmission potential in gastrointestinal nematodes (order: Strongylida).

Microparasite virulence (the potential to cause harm in the host) is thought to be regulated by a direct trade-off with pathogen transmission potential, but it is unclear whether similar trade-offs occur in macroparasites (helminths). In this analysis, the transmission potentials of 5 nematode species (order Strongylida), known to differ in their virulence, were estimated using an index based on egg production and larval survivability. Virulence estimates were based on the minimum number of worms that cause host death. In nematode species where mature adults cause pathology (trichonematidic development), there is a direct relationship between virulence and transmission, suggesting that high virulence is related to parasite fitness in these worms. However, in nematodes where the juvenile stages produce pathology during migration and development (strongylidic development), virulence is not correlated with transmission. These data suggest that trade-offs between transmission and virulence in nematode parasites are not analogous for all species and may depend on the developmental strategy and mechanism of pathogenicity of the parasites.

Intestinal distribution of worms and host ingesta in Nippostrongylus brasiliensis.

The gastrointestinal nematode Nippostrongylus brasiliensis is thought to feed on host ingesta, and it is generally thought that the presence of ingesta determines the distribution of this parasite within the host intestine. However, these assertions have not been supported by direct evidence. The purpose of this study was to test the hypothesis that N. brasiliensis worms are preferentially found in regions of the host small intestine containing ingesta. The relationship between worm and ingesta distribution was investigated using mice infected with N. brasiliensis and killed on day 8 postinfection at 0130, 0730, 1330, or 1930 hr. There was an inverse relationship between worm and ingesta distributions, and the worms were distributed significantly more anteriad in the intestine than host ingesta, at all times during the 24 hr. To determine what the worms fed on, host ingesta, tissue, and blood were differentially labeled with the fluorescent dyes rhodamine B and Fluoresbrite. The results of this study suggest that N. brasiliensis feeds on the host's intestinal wall, and that habitat distribution of this parasite within the small intestine is not directly related to the presence of luminal ingesta.

Role of lipids in the transmission of the infective stage (L3) of Strongylus vulgaris (Nematoda: Strongylida).

Infective larvae (L3) of Strongylus vulgaris have limited energy stores for host finding and for infection. For transmission to occur, the larvae must have sufficient energy to (a) migrate onto grass, where they are ingested by their equine host (host finding), and (b) penetrate into the host gut. This study is designed to test the hypothesis that L3 larvae of S. vulgaris partition their energy stores between locomotory activity (used in host finding) and infection activity (penetration). Chronic locomotory activity was stimulated by incubating S. vulgaris L3 larvae at a constant temperature (38 C). After 8 days of treatment, locomotory activity ceased (exhaustion). Exhausted L3 larvae had significantly decreased total lipid when compared to controls (P < 0.05), but there was no decrease in levels of protein of carbohydrate. Lipids of S. vulgaris L3 larvae are comprised of 9 fatty acids, some of which are depleted in exhausted worms (14:0, 14:1, 16:0, 16:1, 18:1, 18:2), whereas others (18:0, 20:4, 24:0) remain unchanged. These data suggest that specific fatty acids provide the energy source for locomotory activity in S. vulgaris. Exhausted L3 larvae were also less able to penetrate host cecal tissue in in vitro penetration assays when compared to controls (P < 0.05), suggesting that the depletion of individual fatty acids during locomotory activity also reduced infectivity. These data do not support the hypothesis that S. vulgaris L3 larvae partition their energy stores between host-finding and infection activities. A comparison of lipid storage profiles in the L3 larvae of 4 nematode species with similar transmission strategies (S. vulgaris, Strongylus edentatus, Strongylus equinus, and Haemonchus contortus) revealed similarities in the fatty acid composition of these species. These data suggest a relationship between transmission patterns and energy storage strategies in the L3 larvae of nematode parasites of vertebrates.

Villus length influences habitat selection by Heligmosomoides polygyrus.

Heligmosomoides polygyrus is a gastrointestinal nematode whose adult distribution is restricted to the duodenal region in the small intestine of the mouse. This study tests the hypothesis that the habitat of these parasitic worms is influenced by fixed (architectural) cues in the small intestine of the vertebrate host, and that H. polygyrus adults will select microhabitats containing the longest villi. H polygyrus adults attach by coiling around the villi, and longer villi may provide greater attachment resources. In addition, these parasites feed on the epithelial cells covering the villi and thus, longer villi may also provide more food resources. Using histological methods, this study identified a gradient of villus length in the small intestine of the mouse where the longest villi were found in the duodenum and shortest in the ileum. Several non-surgical and surgical treatments were used to differentially alter the overall lengths of the villi. These treatments produced a significant negative correlation between villus length and worm distribution, with the worms selecting regions with the relatively longest villi in the small intestine. Attachment and feeding sites are crucial resources for this parasite, and these data suggest that villus length may be a reliable indicator of resource quality, and that decisions on habitat suitability by H. polygyrus adults may depend on this single, topological variable.

Critical resources that influence habitat selection decisions by gastrointestinal helminth parasites.

Habitat selection may be the basis of some of the most exciting questions in behavioural ecology today, but parasites are being excluded from this debate. Parasites are not aberrant; they form a large proportion of the diversity of life on earth, and one estimate suggests that parasitism is more common than all other feeding strategies combined. We still do not understand the adaptive value of habitat selection behaviours in these organisms, even though the literature is full of examples of parasites migrating and navigating through hosts to their specific habitats. Parasites must make the same decisions that every animal has to make regarding food acquisition, shelter and reproduction. However, we cannot even make reasonable guesses on the habitat selection strategies and critical resources that influence their decision-making. The purpose of this review is to provide examples of experiments and methods of incorporating critical resources into the ecological analyses of habitat selection by gastrointestinal parasites. Information on parasite resources is simply not available for most parasites, and these ideas might stimulate and guide future research. In addition, parasites are ideal models to test theoretical assumptions of habitat selection. Experimental manipulations of parasites are ideal models to test theoretical assumptions of habitat selection. Experimental manipulations of parasite populations are simple, and habitats of endoparasites can be precisely altered by surgical methods. Few tests of habitat selection theory have been attempted in free-living environments because of the difficulty of assessing the correlations between environmental variations and organismal success in real-world situations, but this is not a problem with parasites because their habitats are replicated exactly in each host.

Host grooming and the transmission strategy of Heligmosomoides polygyrus.

Grooming behavior may play a part in the transmission of the gastrointestinal nematode, Heligomosomoides polygyrus in the mouse host. After infective larvae are placed on individually housed mice, significantly higher numbers of adult worms were recovered from the small intestine of mice that were allowed to self-groom when compared to infection levels in mice that had been fitted with Elizabethan collars to prevent self-grooming. Larvae placed on a single mouse housed with 3 other untreated mice resulted in all mice in the group becoming infected, suggesting that allogrooming may also be important in parasite transmission. A significantly higher percentage of larvae nictate on rough surfaces such as damp peat moss substrate when compared to smooth surfaces such as 0.5% agarose. Mice exposed to larvae placed on peat moss substrate have significantly higher infection levels when compared to mice exposed to larvae on a 0.5% agarose substratum, suggesting that natural transmission of infective L3 larvae in mice may be dependent on a substratum type that allows nictation behavior. A significantly higher percentage of worms were attracted to mouse urine and mouse and rat epidermal lipids when compared to deionized water controls in an in vitro preference assay, suggesting an attraction to host-specific signals. These results support the hypothesis that transmission of this parasite is an active process involving movement of the infective larvae of H. polygyrus into the host's active space where they are ingested during grooming behavior.

Mesenchyme cells in Fasciola hepatica (platyhelminthes): primitive glia?

Mesenchyme cells and their processes are found in the cerebral ganglia of the parasitic flatworm, Fasciola hepatica. The mesenchyme cell processes are found in two specialized associations within the ganglion: (i) as lamellae-like multilayer sheaths encircling the cerebral ganglia and separating it from the surrounding parenchyma cells, and (ii) invaginated into the surface of large diameter ('giant') nerve processes to form trophospongium-like relationships. Based on morphological criteria, these mesenchyme cells resemble general invertebrate glial cells suggesting that the mesenchyme cells of these flatworms may represent the earliest glial-like cell.

The food resource of adult Heligmosomoides polygyrus in the small intestine.

The aim of this study was to identify the food resources of Heligmosomoides polygyrus, a gastrointestinal nematode of mice. Gastrointestinal nematodes obtain food from 1 of 3 compartments: host ingesta, blood, or intestinal tissue. A method was developed to label these compartments differentially in the living host using 2 fluorescent marker dyes and to record in situ feeding activity of the parasite. Fluoresbrite is a yellow-green fluorescent dye bound to small-diameter beads that are membrane impermeable. Thus, it is restricted to the bloodstream when introduced there, or it remains in the ingesta when fed to the host. Rhodamine B, a red fluorescent dye, is membrane permeable and stains tissue cytoplasm. These dyes were fed to or injected into the bloodstream of the host. Following treatment, the worms were removed, and the contents of the worm intestines were examined by fluorescent microscopy. Worm intestinal contents only fluoresced with rhodamine B dye. These results suggest that H. polygyrus adults feed on tissue in the living host and not on host ingesta or blood.

FMRFamide-related peptides in Hymenolepis diminuta: immunohistochemistry and radioimmunoassay.

The localization of FMRFamide-related peptide (FaRP) immunoreactivity was determined during different stages of development of the rat tapeworm Hymenolepis diminuta. In the adult worm (14 days old), FaRP immunostaining was most intense in the scolex and concentrated in the central nervous system (cerebral ganglia and transverse commissures) and around the lips of the suckers. In the strobila, medial and lateral longitudinal nerve cords (LNCs) and ladder-like connecting commissures were the only tissue stained. Immunoreactivity in the medial LNCs of the adult tapeworms extended only to and included proglottides containing developing testis and seminal receptacle but disappeared in proglottides in which primordial ovaries were first detected. Radioimmunoassay confirmed that FaRPs were concentrated in the scolex/neck region of the adult worm (3.9 +/- 1.5 pmol mg protein-1), whereas the lowest concentrations (0.2 +/- 0.19 pmol mg protein-1) were recovered from the regions of the strobila containing shelled eggs. The pattern of FaRP immunoreactivity observed in 5- and 7-day-old worms was similar to that seen in adult worms, but in 2- and 3-day-old worms the pattern of immunoreactivity observed in the cerebral ganglia, transverse commissures, and LNCs differed significantly as compared with that seen in older worms. These results indicate differential utilization and/or roles for FaRPs during development and suggest both central and sensory roles in this tapeworm.

Optimal habitat selection by helminths within the host environment.

Helminth parasites of vertebrates usually select very specific regions or habitats in their hosts, and this is often preceded by a tortuous migration through various host organs. However, the proximate mechanisms of migration and habitat selection have remained enigmatic despite considerable effort by parasitologists. In this paper a new approach to studying helminth behaviour in the host is proposed. The core idea is that behaviour strategies must be considered from the perspective of the parasites and their perceptions of their environment. A guiding principle is that the environmental features to which an animal responds, and the actions which are required for responding to the environment, form a fundamental unit of behaviour. Thus, we can deduce an animal's behavioural strategy from the details of its response to environmental signals and from its sensory capabilities. The evidence presented suggests that helminth behaviours in the host often occur as fixed (or modal) action patterns which are usually seen in response to constant, or predictable environmental features. Thus, a working hypothesis is that the mechanisms of physiological and biochemical homeostasis within the host provide an extremely predictable environment for the parasite. Under these conditions, a parasite needs to perceive only small subsets of the total information available from the environment to respond appropriately. Studies on sensory and nervous systems of these organisms are critical to understanding parasite perception, but there are formidable technical obstacles that prevent easy access to parasite nervous systems. Therefore, a multidisciplinary approach, using ideas from parasitology, ecology, evolutionary biology and neuroethology, is considered requisite for reconstructing the parasites' behaviour strategies. It is suggested that future directions should pursue integration of studies on sensory physiology with the behavioural ecology of these organisms.

Intestinal contractions and migration behaviour in Hymenolepis diminuta.

The aim of this study was to determine if intestinal contractions were important in the migration behaviour of the rat tapeworm Hymenolepis diminuta. The objectives were to investigate the intestinal motility responses of the host to a meal which initiates worm migration, and the worms' responses to an artificial peristaltic contraction. A 1 g glucose meal elicited a significant orad migration by H. diminuta in the small intestine of the rat host when compared to water-fed controls (P less than 0.05). The glucose meal also significantly increased the transit rate, and thus, frequency of intestinal contractions in the small intestine of the rat, when compared to water-fed controls (P less than 0.05). Application of a circumintestinal ligature (6.3 g) (simulating an intestinal peristaltic contraction) resulted in significant worm migration when the ligature was applied in regions containing the worm's strobila as compared to controls where loose ligatures were tied in regions containing the strobila, or to controls where tight ligatures were tied ahead of the worm's strobila. These results suggest that H. diminuta migrates in an orad direction in response to the mechanical pressure produced by intestinal contractions induced by host feeding. It is concluded that contractions of the small intestine are an important cue in the migration behaviour of this cestode.

Hymenolepis diminuta: effects of decerebration on thermal response behavior.

Hymenolepis diminuta propels itself with unidirectional peristaltic-like waveforms. When intact adult H. diminuta are placed in a thermal gradient, with the anterior proglottids hot relative to the posterior proglottids, the worms migrate up the gradient toward the hot side. When the anterior is cold, relative to the posterior, the worms moved slightly or little. These behaviors in a thermal gradient represent true thermokinetic responses for an organism with undirectional locomotion. Removal of the scolex, containing the worm's cerebral ganglia, did not significantly alter these thermal responses. These data suggest that the peripheral nervous system is capable of integrating sensory input over the length of the strobila and coordinating locomotory behavior, in the absence of the central nervous system.

Behavioural adaptation of the tapeworm Hymenolepis diminuta to its environment.

Hymenolepis diminuta migrates up the small intestine in response to feeding the host 1 g of glucose. Locomotion during migration may result from fixed patterns of retrograde peristaltic-like waves in the strobila of the tapeworm which propel the organism against the normal expulsive forces in the small intestine. The peristaltic-like locomotory waves occur in a gradient along the strobila with a frequency of 24.9 +/- 0.9 cycles/min in the anterior segments of the worm, decreasing linearly to 6.6 +/- 1.4 cycles/min in the posterior segments of the worm. Chemical signals, isolated from the small intestine of fed hosts, which stimulate migration behaviour in vivo do not alter the behaviour of the scolex or strobila in vitro. Removal of the scolex containing the cerebral ganglia does not alter the frequency or pattern of locomotory activity in the strobila. After the worm is cut into pieces, each region generates the pattern of locomotory activity that is appropriate for that region. These data suggest that the peripheral nervous system, and not the central nervous system, is responsible for the coordination of the fixed patterns of locomotory activity in these tapeworms.