Come with me if you want to live: sympatric parasites follow different transmission routes through aquatic host communities

Community composition, including the relative density of each host species, plays a vital role in the transmission of parasites or disease in freshwater ecosystems. Whereas some host species can effectively transmit parasites, others can act as dead ends (non-viable transmission routes), accumulating large numbers of parasites throughout their life, thus becoming important sinks for parasite populations. Although population sinks have been identified in certain host-parasite systems, robust field estimates of the proportions of parasites that are lost to these hosts are lacking. Here, we quantified the distribution of encysted larval hairworms (phylum Nematomorpha), common parasites in lotic ecosystems, in two subalpine stream communities of New Zealand. With parasite and host population densities calculated per m², we identified which host species most likely contributed to the transmission of three sympatric hairworm morphotypes identified in both streams, and which species acted as population sinks. We also tested for seasonal patterns and peaks in the abundance of each morphotype in the two communities over the sampling season. Finally, we tested whether hosts emerging from the streams had comparable abundances of hairworm morphotypes throughout the sampling period. For each morphotype, different key sets of host species harboured more hairworms on average (abundance) than others, depending on the stream. For one morphotype in particular, two species of hosts were found to be important population sinks that inhibited over a third of these parasites from completing their life cycle. We also observed a clear peak in abundance for another hairworm morphotype during summer. Our data suggest that hosts emerging from the streams matched their aquatic counterparts with respect to hairworm abundance, indicating no infection-dependent reduction in emergence success. Our findings suggest that, depending on relative community composition, sympatric parasites follow different host transmission pathways, some of which lead to dead ends that potentially impact overall infection dynamics. In turn, this information can help us understand the spread or emergence of disease in both freshwater and terrestrial environments, since hairworms infect terrestrial arthropods to complete their life cycle.     

Lake‐derived midges increase abundance of shoreline terrestrial arthropods via multiple trophic pathways

Aquatic insects link adjacent ecosystems by transporting nutrients, energy, and material as they move from bodies of water into terrestrial habitats. Insects emerging from streams and rivers are known to benefit arthropod predators such as spiders, but their influence may extend to other arthropod feeding groups as well. We conducted a terrestrial arthropod survey at a series of lakes spanning a strong gradient of midge (Chironomidae, Diptera) emergence. These small, short‐lived insects reach high densities in some areas such that their carcasses litter the ground, and serve as a potential resource for non‐predatory arthropods. Our study revealed that arthropod assemblages in areas of high midge density were significantly different from those with few midges, the result of an increase of all taxa rather than changes in taxonomic composition. Eight of nine terrestrial arthropod taxa sampled showed a strong positive response to the presence of midges including detritivores and herbivores in addition to predators. Taxa that could consume living or dead midges directly responded especially strongly to midge gradients. Our results strongly suggest that midges enter the terrestrial arthropod food web through multiple pathways, increasing numbers of a wide range of arthropods. Furthermore, they emphasize the importance of lakes as sources of aquatic insects that significantly alter processes in the neighboring terrestrial environment.     

A diverse fossil terrestrial arthropod fauna from New Zealand: evidence from the early Miocene Foulden Maar fossil lagerstätte

Fossil evidence for the evolutionary history of terrestrial arthropods in New Zealand is extremely limited; only six pre‐Quaternary insects (Triassic to Eocene) have been recorded previously, none of Miocene age. The Foulden Maar fossil lagerstätte in Otago has now yielded a diverse arthropod assemblage, including members of the Araneae, Plecoptera, Isoptera, Hemiptera, Coleoptera, Hymenoptera, Trichoptera and Diptera. The fauna significantly emends the fossil record for the Southern Hemisphere, provides an unparalleled insight into a 23‐million‐year‐old New Zealand lake/forest palaeoecosystem and allows a first evaluation of arthropod diversity at a time coeval with or shortly after the maximum marine transgression of Zealandia in the late Oligocene. The well‐preserved arthropods chiefly represent ground‐dwelling taxa of forest floor and leaf litter habitats, mostly from sub‐families and genera that are still present in the modern fauna. They provide precisely dated fossil evidence for the antiquity of some of New Zealand's terrestrial arthropods and the first potential time calibrations for phylogenetic studies. The high arthropod diversity at Foulden Maar, together with a subtropical rainforest flora and fossil evidence for complex arthropod–plant interactions, suggests that terrestrial arthropods persisted during the Oligocene marine transgression of Zealandia.     

Water-seeking behavior in worm-infected crickets and reversibility of parasitic manipulation

One of the most fascinating examples of parasite-induced host manipulation is that of hairworms, first, because they induce a spectacular "suicide" water-seeking behavior in their terrestrial insect hosts and, second, because the emergence of the parasite is not lethal per se for the host that can live several months following parasite release. The mechanisms hairworms use to increase the encounter rate between their host and water remain, however, poorly understood. Considering the selective landscape in which nematomorph manipulation has evolved as well as previously obtained proteomics data, we predicted that crickets harboring mature hairworms would display a modified behavioral response to light. Since following parasite emergence in water, the cricket host and parasitic worm do not interact physiologically anymore, we also predicted that the host would recover from the modified behaviors. We examined the effect of hairworm infection on different behavioral responses of the host when stimulated by light to record responses from uninfected, infected, and ex-infected crickets. We showed that hairworm infection fundamentally modifies cricket behavior by inducing directed responses to light, a condition from which they mostly recover once the parasite is released. This study supports the idea that host manipulation by parasites is subtle, complex, and multidimensional.     

The incidence of bacterial endosymbionts in terrestrial arthropods

Intracellular endosymbiotic bacteria are found in many terrestrial arthropods and have a profound influence on host biology. A basic question about these symbionts is why they infect the hosts that they do, but estimating symbiont incidence (the proportion of potential host species that are actually infected) is complicated by dynamic or low prevalence infections. We develop a maximum-likelihood approach to estimating incidence, and testing hypotheses about its variation. We apply our method to a database of screens for bacterial symbionts, containing more than 3600 distinct arthropod species and more than 150 000 individual arthropods. After accounting for sampling bias, we estimate that 52% (CIs: 48–57) of arthropod species are infected with Wolbachia, 24% (CIs: 20–42) with Rickettsia and 13% (CIs: 13–55) with Cardinium. We then show that these differences stem from the significantly reduced incidence of Rickettsia and Cardinium in most hexapod orders, which might be explained by evolutionary differences in the arthropod immune response. Finally, we test the prediction that symbiont incidence should be higher in speciose host clades. But while some groups do show a trend for more infection in species-rich families, the correlations are generally weak and inconsistent. These results argue against a major role for parasitic symbionts in driving arthropod diversification.     

Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods

Many intracellular micro-organisms are now known to cause reproductive abnormalities and other phenomena in their hosts. The endosymbiont Wolbachia is the best known of these reproductive manipulators owing to its extremely high incidence among arthropods and the diverse host effects it has been implicated as causing. However, recent evidence suggests that another intracellular bacterium, a Cytophaga-like organism (CLO), may also induce several reproductive effects in its hosts. Here, we present the first survey of arthropod hosts for infection by the CLO. We use a sensitive hemi-nested polymerase chain reaction method to screen 223 species from 20 arthropod orders for infection by the CLO and Wolbachia. The results indicate that, although not as prevalent as Wolbachia, the CLO infects a significant number of arthropod hosts (ca. 7.2%). In addition, double infections of the CLO and Wolbachia were found in individuals of seven arthropod species. Sequencing analysis of the 16S rDNA region of the CLO indicates evidence for horizontal transmission of the CLO strains. We discuss these results with reference to future studies on host effects induced by intracellular micro-organisms.     

Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization.

Wolbachia are maternally inherited, intracellular, alpha proteobacteria that infect a wide range of arthropods. They cause three kinds of reproductive alterations in their hosts: cytoplasmic incompatibility, parthenogenesis and feminization. There have been many studies of the distribution of Wolbachia in arthropods, but very few crustacean species are known to be infected. We investigated the prevalence of Wolbachia in 85 species from five crustacean orders. Twenty-two isopod species were found to carry these bacteria. The bacteria were found mainly in terrestrial species, suggesting that Wolbachia came from a continental environment. The evolutionary relationships between these Wolbachia strains were determined by sequencing bacterial genes and by interspecific transfers. All the bacteria associated with isopods belonged to the Wolbachia B group, based on 16S rDNA sequence data. All the terrestrial isopod symbionts in this group except one formed an independent clade. The results of interspecific transfers show evidence of specialization of Wolbachia symbionts to their isopod hosts. They also suggest that host species plays a more important role than bacterial phylogeny in determining the phenotype induced by Wolbachia infection.     

Additions to the checklists of helminth and protozoan parasites of terrestrial mammals and birds in New Zealand

A combined list of additions to previously published checklists of helminth and protozoan parasites of terrestrial mammals and birds in New Zealand is provided. These additions include a total of 21 new host parasite records (11 helminth, 10 protozoan) from 12 mammalian hosts and 82 new records (26 helminth, 56 protozoan) from 43 birds.     

昆虫共生细菌Rickettsia的研究进展

Rickettsia是传播和引起人类与其他脊椎动物疾病的胞内共生菌。引起脊椎动物疾病的这些Rickettsia, 其部分生活史是在节肢动物体内完成的;而另外许多Rickettsia, 其整个生活史都是在宿主节肢动物体内完成。为了叙述方便, 把前者称为脊椎动物Rickettsia, 后者称为节肢动物Rickettsia。过去的研究主要集中在医学上具有重大意义的脊椎动物Rickettsia, 而关于节肢动物Rickettsia的生物学特性等研究则相对较少。近年来, 研究者们加大了对昆虫Rickettsia的研究, 发现昆虫Rickettsia广泛分布于昆虫中, 且有两种存在形式。其可以通过垂直卵传的方式在世代间传递, 也可以通过寄生蜂和寄主植物达到在昆虫之间传播的目的。昆虫Rickettsia可通过诱导孤雌生殖、 诱导杀雄等方式影响宿主的生殖行为。其对不同宿主昆虫可产生对宿主有利或有害的作用;可增强宿主昆虫抵御高温和寄生蜂的能力, 与宿主昆虫对药剂的敏感性相关。最后, 昆虫Rickettsia具有一个简化的基因组, 且存在进一步减小的可能性。     

Absence of <Emphasis Type="Italic">Wolbachia</Emphasis> in Nonfilariid Worms Parasitizing Arthropods

Wolbachia are strictly intracellular maternally inherited α-proteobacteria, largely widespread among arthropods and filariids (i.e., filarial nematodes). Wolbachia capacities to infect new host species have been greatly evidenced and the transfer of Wolbachia between arthropods and filariids has probably occurred more than once. Interestingly, among nematode species, Wolbachia infection was found in filariids but not in closely related lineages. Their occurrence in filariids has been supposed a consequence of the parasitic lifestyle of worms within Wolbachia-infected arthropods, implying that nonfilariid worms parasitizing arthropods are also likely to be infected by some Wolbachia acquired from their hosts. To further investigate this hypothesis, we have examined seven species of nonfilariid worms of Nematoda and Nematomorpha phyla, all interacting intimately with arthropods. Wolbachia infection in nonfilariid parasitic worms was never detected by polymerase chain reaction assays of the 16S rDNA and wsp genes. By contrast, some arthropod hosts are well infected by Wolbachia of the B supergroup. Then the intimate contact with infected arthropods is not a sufficient condition to explain the Wolbachia occurrence in filariids and could underline a physiological singularity or a particular evolutionary event to acquire and maintain Wolbachia infection.     

Parasitic and phoretic arthropods of the elephant-eared and the Santa Cruz kangaroo rats

The parasitic and phoretic arthropods of the elephant-eared kangaroo rat (Dipodomys elephantinus) and Santa Cruz kangaroo rat (D. venustus) are reported; most of these represent new host records. Thirteen of 14 (93%) of D. elephantinus and 11 of 12 (92%) of D. venustus had 11 and nine arthropod species, respectively. Larval and nymphal stages of the tick Dermacentor occidentalis were the most prevalent parasite (77%) on D. elephantinus whereas the mesostigmatid mite Androlaelaps fahrenholzi was the most prevalent (56%) on D. venustus. The arthropod fauna of these two closely related rodents were similar with seven of the 14 arthropod species occurring on both host species. Two species of the host specific listrophorid mite of the genus Geomylichus were found on both hosts.     

Different rates of nucleotide substitutions in Wolbachia endosymbionts of arthropods and nematodes: arms race or host shifts?

The genus Wolbachia encompasses intracellular bacteria found in arthropods and in filarial nematodes. In arthropods, Wolbachia is primarily a reproductive parasite and shows relatively frequent horizontal transfer between host species, while in nematodes it appears to be a mutualist and is strictly vertically transmitted. We can expect that different selective pressures are acting on their genomes. Here we present an analysis of three Wolbachia genes, wsp, ftsZ and dnaA. In wsp of arthropod Wolbachia, an excess of non-synonymous substitutions was observed, providing evidence for positive selection. In nematode Wolbachia, no evidence for positive selection was found. Pressure for amino acid variation in wsp of arthropod Wolbachia could derive either from an arms race with the host or from the occurrence of more frequent hosts shifts due to horizontal transmission. In nematode Wolbachia, the lack of positively selected sites could result from the absence of an arms race, or from the homogeneity of the biochemical environment they exist in (ensured by strict vertical transmission). In ftsZ minor differences in substitution patterns were observed between arthropod and nematode Wolbachia, only in the 3'-portion of the gene. dnaA showed comparable patterns of variation in both lineages, with evidence for strong conservation.     

Bacterial endosymbiont infections in ‘living fossils’: a case study of North American vaejovid scorpions

Bacterial endosymbionts are common among arthropods, and maternally inherited forms can affect the reproductive and behavioural traits of their arthropod hosts. The prevalence of bacterial endosymbionts and their role in scorpion evolution have rarely been investigated. In this study, 61 samples from 40 species of scorpion in the family Vaejovidae were screened for the presence of the bacterial endosymbionts Cardinium, Rickettsia, Spiroplasma and Wolbachia. No samples were infected by these bacteria. However, one primer pair specifically designed to amplify Rickettsia amplified nontarget genes of other taxa. Similar off‐target amplification using another endosymbiont‐specific primer was also found during preliminary screenings. Results caution against the overreliance on previously published screening primers to detect bacterial endosymbionts in host taxa and suggest that primer specificity may be higher in primers targeting nuclear rather than mitochondrial genes.     

Evidence that flatheaded mayflies (Heptageniidae) serve as the likely paratenic host for Chordodes morgani (Nematomorpha) in Nebraska

Hairworms (Nematomorpha) have indirect life cycles that require a terrestrial arthropod definitive host and an aquatic arthropod host that serves as a paratenic host, transferring the hairworm from the aquatic to the terrestrial environment. The life cycles for most hairworms remain unknown, especially the paratenic host. The hairworm Chordodes morgani lays its eggs on sticks, which are susceptible to the activity of aquatic insects such as larvae of the flatheaded mayfly (Heptageniidae), which feed by scraping algae and detritus. To test the likelihood that scrapers serve as the paratenic host for C. morgani, we collected sticks and their accompanying invertebrates from three sites near Lincoln, NE. We noted the presence of eggs of C. morgani on each stick, placed them in labeled resealable bags, and examined the invertebrates microscopically for the presence of hairworm cysts. We predicted that scrapers found on sticks with eggs of C. morgani will harbor the highest number of cysts. To confirm that larvae of the flatheaded mayfly serve as the aquatic host, we fed field-collected specimens to three captive-reared wood roaches (Parcoblatta pensylvanica). Of the three exposed roaches, one yielded nine individuals of C. morgani 63 days after exposure. Understanding the life cycle of this horsehair worm will allow researchers to rear the species in the lab, which could become a model for parasite research.     

Beetles in the diet of six species of deep‐sea fish

Abstract

Four scarab beetles (Acrossidius tasmaniae) and two unidentified weevils were recovered from the guts of a single individual of six deep‐sea fishes trawled from depths of 326–418 m, c. 30–40 km off the Wairarapa coast, North Island, New Zealand. These constitute the first records of terrestrial arthropods in the diet of deep‐sea fishes from the New Zealand region. Possible reasons describing how these terrestrial beetles came to be eaten by these fishes are discussed.     

New records of nematomorph parasites (Nematomorpha: Gordiida) of ground beetles (Coleoptera: Carabidae) and camel crickets (Orthoptera: Rhaphidophoridae) in Washington State

From 1998 to 2003, beetles and crickets infected with hairworms were collected from 4 localities within the Hanford Nuclear Site and the Hanford Reach National Monument, located in a shrub-steppe region of Washington State along the Columbia River. Infected hosts comprised 6 species of carabid beetles within 5 genera and 2 camel crickets within 1 genus; all are newly documented insect-nematomorph associations. A large proportion of the infected hosts (48%) were collected from a single site during a single collecting period. Of the 38 infected hosts, 32 contained a single worm, 4 hosts contained 2 worms, and 2 hosts contained 3 worms. Five of the hosts with multiple infections contained at least 1 male and 1 female worm. Camel crickets were infected with Neochordodes occidentalis while carabids were infected with an undescribed species of Gordionus . As the majority of hairworms are collected in the post-parasitic adult phase, host data and hairworm-arthropod associations remain poorly documented and our work adds new data to this area of nematomorph biology.     

Metabarcoding as a tool for investigating arthropod diversity in Nepenthes pitcher plants

The biodiversity of tropical forests consists primarily of small organisms that are difficult to detect and characterize. Next‐generation sequencing (NGS) methods can facilitate analyses of these arthropod and microbial communities, leading to a better understanding of existing diversity and factors influencing community assembly. The pitchers of carnivorous pitcher plants often house surprisingly discrete communities and provide ideal systems for analysis using an NGS approach. The plants digest insects in order to access essential nutrients while growing in poor soils; however, the pitchers are also home to communities of living organisms, called inquilines. Certain arthropods appear to have coevolved with their pitcher plant hosts and are not found in other environments. We used Illumina amplicon sequencing of 18S rDNA to characterize the eukaryotes in three species of Nepenthes (Nepenthaceae) pitcher plants – N. gracilis, N. rafflesiana and N. ampullaria – in each of three different parks in Singapore. The data reveal an unexpected diversity of eukaryotes, significant differences in community diversity among host species, variation in host specificity of inquilines and the presence of gregarine parasites. Counts of whole inquiline arthropods from the first collection year were roughly correlated with scaled 18S sequence abundances, indicating that amplicon sequencing is an effective means of gauging community structure. We barcoded a subset of the dipteran larvae using COI primers, and the resulting phylogenetic tree is mostly congruent with that found using the 18S locus, with the exception of one of five morphospecies. For many 18S and COI sequences, the best BLASTn matches showed low sequence identity, illustrating the need for better databases of Southeast Asian dipterans. Finally, networks of core arthropods and their host species were used to investigate degree of host specificity across multiple hosts, and this revealed significant specialization of certain arthropod fauna.     

Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae)

The maintenance of strict host specificity by parasites when several closely related host species live in sympatry is poorly understood. Species of intertidal trochid snails in the genera Diloma, Melagraphia and Austrocochlea often occur together and are parasitised by a single digenean morphotype (Platyhelminthes, Trematoda), tentatively placed in Opecoelidae. Of the 10 trochid species (6 from New Zealand, 4 from Australia) we examined, six were found to be infected, and the prevalence of infection was as high as 17.5%. We obtained molecular data (mitochondrial 16S and nuclear rDNA internal transcriber spacer 2 sequences, representing 774 bp), to infer phylogenetic relationships amongst these Digenea. Our phylogeny separated the single morphotype into three clearly defined clades (which are almost certainly separate biological species): (i) those infecting two species of Austrocochlea from Tasmania, (ii) those infecting Diloma subrostrata in Otago and Southland, New Zealand, and (iii) those infecting all the parasitised New Zealand topshells (Melagraphia aethiops, D. subrostrata, Diloma nigerrima and Diloma arida) throughout the country. This last group comprised two subclades, one infecting only D. subrostrata and one infecting the other three species. Two D. subrostrata populations were each found to be infected by genetically distinct parasites, yet sympatric populations of the other snails were not necessarily infected. This study is thus the first to reveal cryptic species of digeneans in a single population of a molluscan first intermediate host. We point out also that the degree of host specificity would have been grossly underestimated if, in the absence of our genetic analysis, we had only considered digenean morphology. Our results shed light on the conditions that may favour switching among intermediate hosts in digeneans, and on the presence/absence of host specificity in these parasites.     

The origin and evolution of parasitism on terrestrial vertebrates in insects, mites, and ticks

Coexistence of terrestrial vertebrates and arthropods has been continuing over 200 million years; various forms of parasitism originated independently in various groups of arthropods during this period. The association of Acari and insects with nests and shelters of their hosts (nidicoly) played the main role in the origin of parasitism in these major groups of arthropods. The primary step in the evolution of parasitism was the permanent habitation in nests and borrows of mammals and birds in Mesozoic era. The second step was a substitution of various forms of schizophagy by the regular feeding on products of vital activity and dead parts of host body. The next step was the feeding on various body parts of vertebrate hosts, namely skin, hair, feathers, external excreta, and drops of blood. The final step was the development of the ability to damage skin and suck out the blood of vertebrates. In some taxa of astigmatid mites the parasitism on birds originated from phoresy: hypopi (heteromorphous deutonymphs) obtained the ability to absorb the liquid nutrients from hair follicles and subcutaneous tissues through the cuticle. The development of haematophagous feeding on mammals in several families of Diptera was the second way of the origin of parasitism. Highly mobile dipterans with the piercing-sucking or licking mouthparts were able to change easily from the accidental puncturing of the host skin or licking of the blood, pus, and mucus to the obligatory haematophagy. The evolution of some arthropod taxa did not went beyond a primary domination of spatial relations, as in many astigmatid mites, or trophic relations in the form of micropredatory, as in the haematophagous Diptera.