Punch in the gut: parasite tolerance of phytochemicals reflects host diet

Gut parasites of plant-eating insects are exposed to antimicrobial phytochemicals that can reduce infection. Trypanosomatid gut parasites infect insects of diverse nutritional ecologies as well as mammals and plants, raising the question of how host diet-associated phytochemicals shape parasite evolution and host specificity. To test the hypothesis that phytochemical tolerance of trypanosomatids reflects the chemical ecology of their hosts, we compared related parasites from honey bees and mosquitoes – hosts that differ in phytochemical consumption – and contrasted our results with previous studies on phylogenetically related, human-parasitic Leishmania. We identified one bacterial and 10 plant-derived substances with known antileishmanial activity that also inhibited honey bee parasites associated with colony collapse. Bee parasites exhibited greater tolerance of chrysin – a flavonoid found in nectar, pollen and plant resin-derived propolis. In contrast, mosquito parasites were more tolerant of cinnamic acid – a product of lignin decomposition present in woody debris-rich larval habitats. Parasites from both hosts tolerated many compounds that inhibit Leishmania, hinting at possible trade-offs between phytochemical tolerance and mammalian infection. Our results implicate the phytochemistry of host diets as a potential driver of insect–trypanosomatid associations and identify compounds that could be incorporated into colony diets or floral landscapes to ameliorate infection in bees.     

Asymmetric competition between distant taxa: poecilid fishes and water striders

Summary Competition for water surface prey between fish (Priapichtus annectens: Poeciliidae) and water striders (Potamobates unidentatus: Gerridae) was studied in the laboratory and in pools in a small tropical stream. Laboratory experiments showed that fish depressed activity and foraging success of water striders. Large fish (4–5 cm) had a greater effect than small fish (2–3 cm). The field experiment showed that competition was highly asymmetric. Presence of fish decreased water strider foraging success while the reverse interaction was insignificant. It is suggested that the higher individual foraging success of the fish, harassment of water striders by fish and the use of an exclusive resource, benthic invertebrates, by the fish, contribute to this pattern. Habitat use differed between the two species. Fish used the deeper parts of stream pools and water striders used the shallower parts of the pools. Asymmetric interference and exploitation competition may force water striders to use shallow edge habitats.     

Influence of gut parasites on growth performance in the water strider Gerris buenoi (Hemiptera: Gerridae)

Water striders harbor a diverse assemblage of symbionts in their digestive tract We used a field experiment, in which water striders were reared in enclosures in their natural pond habitat, to assess the effects of gut symbionts on growth Trypanosomatid flagellates had significant adverse effects on both development time and adult size, and therefore are clearly parasitic Yet because of their low prevalences (2% or less), trypanosomatids cannot be a major factor in the dynamics of our study population Gregannes occurred in 36% of the water striders, often in high numbers, and filling the entire midgut of some bugs Nevertheless, infected and uninfected gerrids did not differ in their growth, and gregarine loads were uncorrelated with development time and adult size attained We also did not find effects of gregarines in a second experiment with different rearing conditions, including a treatment with food stress We used a quantitative genetic approach to test if resistance against gregarines has a heritable component There was no evidence for any genetic variation, suggesting that variability in gregarine loads is the result of environmental heterogeneity Comparison with published reports from water striders shows that there is a great variability in the diversity and prevalence of symbionts among different populations and species, of gerrids     

Fishing spiders, green sunfish, and a stream-dwelling water strider: male-female conflict and prey responses to single versus multiple predator environments

Many studies have experimentally addressed the effects of a particular predator species on prey behavior. In nature, however, prey frequently face multiple species of predators that often vary in their predatory mode and in their level of predation risk. Relatively few studies have considered prey responses under these complex conditions. In Kentucky, the stream-dwelling water strider (Aquariusremigis) coexists with many potentially dangerous predators, two of which are the green sunfish (Lepomiscyanellus) and the fishing spider (Dolomedesvittatus). Green sunfish occupy stream pools and attack water striders from below. In contrast, fishing spiders hunt along stream shorelines where they perch on overhanging vegetation or rocks and attack water striders near shore. We compared how A. remigis individuals respond to these two very different predators in pools with one or both predators. The presence of sunfish in pools had strong effects on male water strider behavior, including increased use of three types of refuge from sunfish (riffles, climbing out of the water, sitting on the water but at the edges of pools), decreased activity and a decreased number of aggressive males on the water. Spiders also influenced water strider behavior; male water striders avoided spiders by shifting away from the edges of pools. Comparisons of the effects of the two predator species showed that in general, antipredator responses by male water striders were stronger in pools with fish alone than in those with spiders alone. In the presence of both predators, male water strider behavior (microhabitat use and activity) was generally similar to behavior in the presence of fish alone. In contrast, female water striders showed no significant response to the presence of sunfish, and little response to the presence of spiders. This lack of response could be because females spent much of their time in refuges even in the absence of predators (apparently hiding from harassment by males). Both spiders and fish caused decreases in water strider mating activity. The presence of fish reduced both the number of matings per pool (mating frequency), and mean mating durations. Spiders induced a decrease in mean mating duration, but not in mating frequency. The largest reductions in mating activity occurred in pools with both predators present. Pools with either spiders or fish alone suffered 15–20% water strider mortality during our experiment (versus no mortality in predator-free pools). Extant theory suggests that when prey face conflicting microhabitat responses to two predators (as in this study), the predators should have facilitative effects on predation rates (i.e., prey that avoid one predator are often killed by the other and vice versa). Mortality rates in pools with both predators present, however, were not significantly different from that predicted by a null model of multiple predator effects. The lack of predator facilitation can be explained by the compensatory reductions in water strider activity and mating activity in the presence of both predators. Received: 26 August 1996 / Accepted: 12 June 1998     

Spatial structure-mediated indirect effects of an aquatic plant, Trapa japonica, on interaction between a leaf beetle, Galerucella nipponensis, and a water strider, Gerris nepalensis

The spatial structure-mediated indirect effects of an aquatic host plant, Trapa japonica (Trapaceae), on survival of a leaf beetle, Galerucella nipponensis (Coleoptera: Chrysomelidae), with regard to predation by a water strider, Gerris nepalensis (Hemiptera: Gerridae), were investigated in an irrigation pond and under indoor conditions. Beetle density, particularly in the first-instar stage of the larvae, became extremely low in the second generation in the pond, even though food resources were abundant. The biological check method, which excludes natural enemies by caging, suggested that a causal factor of the low density was predation by Gerris nepalensis in midsummer and thereafter. Normally growing rosettes extend their leaves horizontally on the water surface. However, some rosettes of T. japonica grew leaves vertically in the later seasons, and such overgrown rosettes were distributed patchily in the ponds. Beetle density was higher on the latter rosettes than on the former ones. The indoor experiment showed that the water strider can feed on the eggs of beetles on normally grown rosettes but not on the overgrown rosettes. Furthermore, female adults of Galerucella nipponensis preferred the overgrown rosettes over the normally grown rosettes for oviposition when water striders were present. These facts suggest that the spatial structure-mediated indirect effects of the host plant modify the interaction between herbivore and predator. Received: November 22, 2001 / Accepted: February 26, 2002     

Predation versus resource limitation in survival of adult burrowing wolf spiders (Araneae: Lycosidae)

Summary The influences of food supply and density on adult survival were examined in the burrowing wolf spider Geolycosa rafaelana (Lycosidae), using manipulations of spider populations on eight 400 sq m experimental plots. A total of 110 adult spiders were captured, weighed, marked, and returned to their burrows during April–May 1983. Treatments of (1) food supplementation, (2) density reduction, (3) food supplementation combined with density reduction, and (4) no manipulation (control) were applied to the eight populations, and adult survival and reproduction were monitored during May–October 1983. Survival rates were higher for nonreproducing adult female populations with reduced density, and lower for nonreproducing females in populations with food supplementation. A pompilid wasp, Paracyphononyx funereus, was documented as a parasitoid of G. rafaelana, producing 50%–65% mortality in adult females during winter, and 4–5% mortality in adult females during summer. The observed survival responses were correlated with variations in predation, while parasitism did not appear to be strongly density-dependent.     

Experiments on the effects of food and density on voltinism in a stream-dwelling water strider (Aquarius remigis)

1. The stream water strider Aquarius remigis shows a latitudinal pattern of variation in voltinism. In general, populations with shorter growing seasons (e.g. in eastern Canada) tend to be univoltine (animals that reach adulthood in the summer overwinter before reproducing in the following spring), whereas populations with somewhat longer growing seasons (e.g. in the north-eastern United States) tend to be bivoltine. 2. This pattern was broken at our study site in the south-eastern United States (Kentucky) where A. remigis had a long growing season, but was almost always univoltine. In summer 1993, however, adult A. remigis in central Kentucky displayed a bivoltine reproductive cycle; i.e. individuals in some pools began breeding shortly after maturing to the adult stage. 3. A field survey documented a negative relationship between local water strider density and reproductive activity in prediapause adults. A laboratory experiment manipulating food availability and density, revealed that animals held at low density with high food levels displayed greater mating activity and egg production than did their counterparts at higher density or lower food levels. 4. A laboratory experiment also showed that high water strider density resulted in a greater frequency of very short pair durations (< 10 min). 5. Although the observed effects of density and food availability on mating activity of prediapause adults seem intuitively reasonable, they differ from the patterns observed in overwintered adults. The difference in reproduction patterns might be due to differences in selective pressures on prediapause vs. post-diapause adults.     

Temperature dependence of parasitic infection and gut bacterial communities in bumble bees

High temperatures (e.g., fever) and gut microbiota can both influence host resistance to infection. However, effects of temperature-driven changes in gut microbiota on resistance to parasites remain unexplored. We examined the temperature dependence of infection and gut bacterial communities in bumble bees infected with the trypanosomatid parasite Crithidia bombi. Infection intensity decreased by over 80% between 21 and 37°C. Temperatures of peak infection were lower than predicted based on parasite growth in vitro, consistent with mismatches in thermal performance curves of hosts, parasites and gut symbionts. Gut bacterial community size and composition exhibited slight but significant, non-linear, and taxon-specific responses to temperature. Abundance of total gut bacteria and of Orbaceae, both negatively correlated with infection in previous studies, were positively correlated with infection here. Prevalence of the bee pathogen-containing family Enterobacteriaceae declined with temperature, suggesting that high temperature may confer protection against diverse gut pathogens. Our results indicate that resistance to infection reflects not only the temperature dependence of host and parasite performance, but also temperature-dependent activity of gut bacteria. The thermal ecology of gut parasite-symbiont interactions may be broadly relevant to infectious disease, both in ectothermic organisms that inhabit changing climates, and in endotherms that exhibit fever-based immunity.     

Ecological energetics of Central European grasshoppers (Orthoptera: Acrididae)

Summary Biomass and energy budgets and food utilization efficiencies of laboratory and wild populations of three Central European grasshopper species, Chorthippus parallelus (Zetterstedt), C. biguttulus (L.), and Gomphocerus rufus (L.), were studied between 1979 and 1984. Larval consumption is relatively low in C. biguttulus (C=4.3 kJ/ind.) compared with C. parallelus and G. rufus (4.9 kJ/ind.). In the adult phase (maturity) consumption rates of C. biguttulus and G. rufus (6.9 kJ/ind.) are similar, but higher in C. parallelus (7.3 kJ/ind.). The energy content decreases from the egg (23.2–24.3 J/mg dw) and body tissue (22.1–23.2 J/mg dw) to faeces (16.6–18.1 J/mg dw). The energy contents of faeces differ significantly between the species, indicating different rates of food conversion (on Dactylis glomerata). On average, the assimilation rates are about 30%, slightly lower in G. rufus. Approximate digestibility (A/C) ranges from 28.2 (G. rufus) to 35.7 (C. biguttulus) without great differences between larvae and adults. In contrast, the efficiency of conversion of ingested food (P/C) differs significantly between larval (10–11) and adult stages (3.4–3.6), and so to a much higher degree does the efficiency of conversion of digested food (P/A), from 30.3–33.5 in the larval to 9.5–14.9 in the adult period. Based on 5-year (C. parallelus) and 2-year studies (G. rufus) of the population dynamics and life tables, the energy budgets of wild populations were calculated and summarized into diagrams. Depending on the annually fluctuating densities, in both populations about 1%–2% of net primary production was consumed, and another 5%–9% was cut and dropped. The proportion of production of the grasshopper populations (body tissue) used for egg production differs in C. parallelus (28%) and G. rufus (44%). The energy cycling owing to energy storage in the living eggs amounts to 2%–3% of the total energy consumed by the population. The results are compared with the available data for grasshoppers in the literature.     

Megafauna associations with deepwater corals (Primnoa spp.) in the Gulf of Alaska

Our study showed that one species of water strider (Aquarius najas) dominated the insect fauna (>90% of the biomass) on and near the surface of a small stream in southern Sweden, but the diet of Daubenton's bats (Myotis daubentonii), regularly feeding over the same stream, contained <1% of these insects. To explain why the bats did not eat water striders in proportion to the apparent abundance of these insects, we tested three hypotheses, with the following results: (1) The water striders did not respond to artificial bat calls and therefore their defence against bats is not based on ultrasonic hearing. (2) Water striders hand-fed to the bats were eaten with similar frequency as palatable controls (caddis flies), so there is no evidence that water striders are unpalatable to bats. (3) Attempted prey-captures by the bats occurred less often than expected within 1 m of the bank of the stream (the bank consisted of a stone wall), indicating that the bats' flight or, alternatively, their detection or capture of insects, was difficult within that area, possibly constrained by clutter. At dusk and just before the bats emerged to feed, the water striders moved away from the open water. They remained motionless close to the bank for as long as the bats were active.     

The more insect trypanosomatids under study-the more diverse Trypanosomatidae appears

From 10 trypanosomatids genera six comprise monogenetic parasites of insects and for the rest of four genera insects may serve as vectors. The invertebrate host is an essential element of trypanosomatids life cycle, but from more than 900 recognised vertebrate hosts only about 500 species of insects have been discovered to be the hosts of homoxenous trypanosomatids. Nothing or very little is known about insect trypanosomatids in many extensive areas such as South East Asia, Australia, Japan and some others. Each new region explored brings many new findings. Recently flagellates were found in new insect species and families. The border of parasites distribution was expanded till Central Asia, Far East and North over the Polar Circle. As paleogeographical events are now under contemplating in trypanosomatids phylogeny researches so northern insect trypanosomatids may attract some attention as the elements of postglacial fauna which is definitely young. Very broad host specificity of insect trypanosomatids and high probability to isolate non-specific parasite show causes that only the investigation of a culture may solve the question 'what parasite was really isolated?'. Examination of cell morphotypes in the host has clearly demonstrated that they are not sufficient for classification and may lead us to be mistaken. The number of insect trypanosomatid cultures is inadequate for characterisation of the diversity of insects trypanosomatids. Trypanosoma is actually the only trypanosomatid genus which is out of questions. Insect trypanosomatids comprise the most diversified part of trypanosomatids evolutionary tree. Recent ssrRNA phylogenetic analysis and morphological data show that three insect isolates represent new lineages on trypanosomatid evolutionary tree, as well as dendrograms derived from PCR data demonstrated some new groups of isolates. Therefore, the more insect trypanosomatids are involved in laboratory investigations--the more new clusters or/and new lineages are appearing on the tree.     

Leptomonas lactosovorans n. sp., a Lactose-Utilizing Trypanosomatid: Description and Nutritional Requirements1

Leptomonas lactosovorans n. sp. is described from the gut of the reduviid hemipteran Zelurus martinsi. It can be grown in a defined medium. The requirements for amino acids, vitamins, purine, and heme were similar to those established for Crithida fasciculata. Growth is stimulated by aeration. Generation time is longer than for any other insect trypanosomatid described; its utilization of lactose as a carbon source is a unique feature among trypanosomatids.     

Host resistance and tolerance of parasitic gut worms depend on resource availability

Resource availability can significantly alter host–parasite dynamics. Abundant food can provide more resources for hosts to resist infections, but also increase host tolerance of infections by reducing competition between hosts and parasites for food. Whether abundant food favors host resistance or tolerance (or both) might depend on the type of resource that the parasite exploits (e.g., host tissue vs. food), which can vary based on the stage of infection. In our study, we evaluated how low and high resource diets affect Cuban tree frog (Osteopilus septentrionalis) resistance and tolerance of a skin-penetrating, gut nematode Aplectana sp. at each stage of the infection. Compared to a low resource diet, a high resource diet enhanced frog resistance to worm penetration and tolerance while worms traveled to the gut. In contrast, a low resource diet increased resistance to establishment of the infection. After the infection established and worms could access food resources in the gut, a high resource diet enhanced host tolerance of parasites. On a high resource diet, parasitized frogs consumed significantly more food than non-parasitized frogs; when food was then restricted, mass of non-parasitized frogs did not change, whereas mass of parasitized frogs decreased significantly. Thus, a high resource diet increased frog tolerance of established worms because frogs could fully compensate for energy lost to the parasites. Our study shows that host–parasite dynamics are influenced by the effect of resource availability on host resistance and tolerance, which depends on when parasites have access to food and the stage of infection.     

Use of glycoconjugates for trypanosomatid taxonomy

Glycoconjugates from five trypanosomatid genera—Crithidia, Herpetomonas, Endotrypanum, Leishmania, and Trypanosoma—were extracted with Triton X-114 and analyzed by sodium dodecyl sulfate polyacrylamide gel electrophoresis followed by periodic acid-Schiff staining. Most of the glycoconjugates were detected in the hydrophobic phase, indicating the presence of anchored glycoconjugates. All the trypanosomatids expressed a glycoconjugate with a low molecular weigh (below 20 kDa) in this phase. In each species, however, a characteristic and specific pattern of glycoconjugates was also observed in both phases. In the hydrophobic phase: 14–29 kDa lycoconjugates in C. guilhermei; 24–70 kDa in C. fasciculata, C. luciliae, E. schaudinni, and T. cruzi Y and G strains; 45–66 kDa in C. oncopelti and H. samuelpessoai; above 36 kDa in T. dionisii; 20–24 kDa, 36–45 kDa, and 70 kDa in L. tarentolae and T. mega. In the hydrophilic phase, typical glycoproteins were observed in some trypanosomatids: 60 kDa in T. mega and T. cruzi Y strain; 70 kDa in H. samuelpessoai; 66 kDa in C. oncopelti; 20–70 kDa in C. luciliae. These findings suggest that Triton X-114-extracted glycoconjugates could be useful markers for trypanosomatid taxonomy.     

Mate disruption in the water strider Aquaris remigis Say, 1832 (Hemiptera: Gerridae)

This report describes the behaviour of a previously uncharacterised mating tactic amongst male water striders (Aquarius remigis Say, 1832), involving the physical break up of existing mating pairs. Using data from four separate laboratory observations on the water strider mating system, we show that this behaviour represents roughly 12.6% of all mating attempts by males. Furthermore, we demonstrate that males are successful in breaking up the existing mating pair in 15.6% of the cases, resulting in secure matings with the disrupted female 6.2% of time. We suspect that mate disruption may serve as an alternative means for acquiring mates by males with low mating success using conventional behaviours. Further research should be performed to determine the prevalence of this behaviour in various natural populations and the specific contexts in which this behaviour occurs.     

High Prevalence and Endemism of Trypanosomatids on a Small Caribbean Island

We describe the monoxenous trypanosomatids parasitizing true bugs and flies on the island of Curaçao. Out of 248 examined true bugs belonging to 17 species, 93 individuals were found to be infected (overall 38% prevalence) by at least one trypanosomatid species (referred to as typing units; TUs). Out of 80 flies, six were infected. All detected trypanosomatids were compared based on their 18S rRNA sequences with TUs parasitizing bugs and flies described from mainland South America, allowing us to assess their diversity and distribution. Besides Leptomonas pyrrhocoris and Leptomonas seymouri, two known species of the subfamily Leishmaniinae, our analysis revealed six new TUs falling into the groups ‘jaculum’, Blastocrithidia and Herpetomonas. Moreover, two new members of the genus Phytomonas and three new TUs belonging to the monophyletic group designated as ‘new clade II’ sensu Mol. Phylogenet. Evol, 69, 255 (2013) were isolated. The detected trypanosomatids were characterized by moderate diversity (13 TUs) species richness. Out of nine and four TUs from the heteropteran and dipteran hosts, respectively, 11 TUs have not been encountered before. Although a sampling bias may partially affect the comparison between trypanosomatid communities on Curaçao and the mainland, the high proportion of unique TUs from the former location suggests that the prominent role of islands in increasing the global diversity of macroscopic organisms may also extend to their protistan parasites.     

An elemental and stable isotope assessment of water strider feeding ecology and lipid dynamics: synthesis of laboratory and field studies

1. Despite the ubiquity and abundance of water striders (Hemiptera: Gerridae) in temperate streams and rivers and their potential usefulness as sentinels in contaminant studies, little is known about their feeding ecology and lipid dynamics. 2. In this study we used stable isotopes of carbon (δ¹³C) and nitrogen (δ¹⁵N) and elemental carbon to nitrogen ratios (C/N) to assess dietary habits and lipid content, respectively, for water striders. 3. To determine diet‐tissue fractionation factors, nymphs of the most common species in New Brunswick, Canada, Aquarius remigis were reared in the laboratory for 73 days and exhibited rapid isotopic turnover in response to a switch in diet (C half‐life = 1.5 days, N half‐life = 7.8 days). Their lipid content increased towards the end of the growing season and resulted in lower δ¹³C values. Diet‐tissue fractionation factors were established after correction of δ¹³C data for the confounding effect of de novo lipid synthesis (strider δ¹³C_adj– diet δ¹³C_adj = 0.1‰, strider δ¹⁵N – diet δ¹⁵N = 2.7‰). 4. Water striders from the majority of 45 stream sites (83%) in New Brunswick had less than 50% contribution of aquatic carbon to their diets but showed a gradual increase in the contribution of this carbon source to their diet with increasing stream size. 5. These data indicate that striders exhibit a strong connection to terrestrial carbon sources, making them important users of energy subsidies to streams from the surrounding catchment. However, this dependence on terrestrial organic matter may limit their utility as indicators of contamination of aquatic systems by heavy metals and other pollutants.     

Role of body size in dominance interactions between male water striders, Aquarius paludum

Water striders are a model system for the study of sexual size dimorphism, but the effect of body size on the dominance relationship between individuals has not been experimentally tested. In 34 staged contests between males of the water strider Aquarius paludum, we determined the effect of body size difference between contestants on the outcome of the aggressive interactions. In contests between a large and a small male, the larger individuals won the interactions significantly more often than expected by chance. This is the first experimental evidence for the importance of body size in pair-wise contests among water striders.     

Discovery and barcoding by analysis of spliced leader RNA gene sequences of new isolates of Trypanosomatidae from Heteroptera in Costa Rica and Ecuador

Trypanosomatid diversity in Heteroptera was sampled using a culture-independent approach based on amplification and sequencing of Spliced Leader RNA gene repeats from environmental samples. By combining the data collected herein with that of previous work, the prevalence of parasites was found to be 22%-23%. Out of approximately 170 host species investigated nearly 60 were found to harbor trypanosomatids. The parasites found were grouped by cluster analysis into 48 typing units. Most of these were well separated from the known groups and, therefore, likely represent new trypanosomatid species. The sequences for each typing unit serve as barcodes to facilitate their recognition in the future. As the sampled host species represent a minor fraction of potential hosts, the entire trypanosomatid diversity is far greater than described thus far. Investigations of trypanosomatid diversity, host-specificity, and biogeography have become feasible using the approach described herein.     

Transovum Transmission of Trypanosomatid Cysts in the Milkweed Bug,Oncopeltus fasciatus

Leptomonas wallacei is a trypanosomatid that develops promastigotes and cystic forms in the gut of the hemipteran insect Oncopeltus fasciatus. Insect trypanosomatids are thought to be solely transmitted from one host to another through the ingestion of parasite-contaminated feces. However, here we show that L. wallacei cysts present on the eggshells of eggs laid by O. fasciatus can also act as infective forms that are transmitted to the insect offspring. Newly hatched O. faciatus nymphs are parasite-free, but some of them become contaminated with L. wallacei after feeding on eggshell remnants. The present study is the first report of transovum transmission of a trypanosomatid, a process that may have a relevant role in parasite’s within-host population dynamics.