Nematode Parasites of Vertebrates: Their Development and Transmission

Animals experience varying levels of predation risk as they navigate heterogeneous landscapes, and behavioral responses to perceived risk can structure ecosystems. The concept of the landscape of fear has recently become central to describing this spatial variation in risk, perception, and response. We present a framework linking the landscape of fear, defined as spatial variation in prey perception of risk, to the underlying physical landscape and predation risk, and to resulting patterns of prey distribution and antipredator behavior. By disambiguating the mechanisms through which prey perceive risk and incorporate fear into decision making, we can better quantify the nonlinear relationship between risk and response and evaluate the relative importance of the landscape of fear across taxa and ecosystems.

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Landscapes of Fear: Spatial Patterns of Risk Perception and Response

The COVID-19 pandemic has resulted in unparalleled global impacts on human mobility. In the ocean, ship-based activities are thought to have been impacted due to severe restrictions on human movements and changes in consumption. Here, we quantify and map global change in marine traffic during the first half of 2020. There were decreases in 70.2% of Exclusive Economic Zones but changes varied spatially and temporally in alignment with confinement measures. Global declines peaked in April, with a reduction in traffic occupancy of 1.4% and decreases found across 54.8% of the sampling units. Passenger vessels presented more marked and longer lasting decreases. A regional assessment in the Western Mediterranean Sea gave further insights regarding the pace of recovery and long-term changes. Our approach provides guidance for large-scale monitoring of the progress and potential effects of COVID-19 on vessel traffic that may subsequently influence the blue economy and ocean health.

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Tracking the global reduction of marine traffic during the COVID-19 pandemic.

Predators often cause prey to adopt defensive strategies that reduce predation risk. The ‘ecology of fear’ examines these trait changes and their consequences. Similarly, parasites can cause hosts to adopt defensive strategies that reduce infection risk. However the ecological and evolutionary consequences of these behaviors (the ‘ecology of disgust’) are seldom considered. Here we identify direct and indirect effects of parasite avoidance on hosts and parasites, and examine differences between predators and parasites in terms of cost, detectability, and aggregation. We suggest that the nonconsumptive effects of parasites might overshadow their consumptive effects, as has been shown for predators. We emphasize the value of uniting predator–prey and parasite–host theory under a general consumer–resource framework.

Ecological and Evolutionary Consequences of Parasite Avoidance.

A global parasite conservation plan

Nearly half of all animals may have a parasitic lifestyle, yet the number of transitions to parasitism and their potential for species diversification remain unresolved. Based on a comprehensive survey of the animal kingdom, we find that parasitism has independently evolved at least 223 times in just 15 phyla, with the majority of identified independent parasitic groups occurring in the Arthropoda, at or below the level of Family. Metazoan parasitology is dominated by the study of helminthes; however, only 20% of independently derived parasite taxa belong to those groups, with numerous transitions also seen in Mollusca, Rotifera, Annelida and Cnidaria. Parasitism is almost entirely absent from deuterostomes, and although worm-like morphology and host associations are widespread across Animalia, the dual symbiotic and trophic interactions required for parasitism may constrain its evolution from antecedent consumer strategies such as generalist predators and filter feeders. In general, parasitic groups do not differ from their free-living relatives in their potential for speciation. However, the 10 largest parasitic clades contain 90% of described parasitic species, or perhaps 40% of all animal species. Hence, a substantial fraction of animal diversity on the Earth arose following these few transitions to a parasitic trophic strategy.

https://royalsocietypublishing.org/doi/pdf/10.1098/rsbl.2016.0324

Independent origins of parasitism in Animalia.

A rancid meal, a moist handshake, a pile of feces: These phenomena elicit disgust and avoidance that protect humans from our most pervasive consumer—infectious agents. This avoidance is not specific to humans. Various animals alter their behavior to avoid infection ( 1 ). For instance, Poirotte et al. recently showed that mandrills avoid parasite-contaminated feces and refrain from grooming infected individuals ( 2 ). These primates' nuanced ability to detect and alter their behavior in response to differential exposure risk suggests close parallels to the “landscape of fear” elicited by predators (see the figure), with perceived peaks and valleys driven by parasite abundance and exposure risk.

http://science.sciencemag.org/content/sci/359/6381/1213.full.pdf

A landscape of disgust.

Fear of predation alters prey behavior, which can indirectly alter entire landscapes. A parasite‐induced ecology of fear might also exist if animals avoid parasite‐contaminated resources when infection costs outweigh foraging benefits. To investigate whether animals avoid parasite contaminated sites, and if such avoidance balances disease costs and foraging gains, we monitored animal behavior at raccoon latrines – sites that concentrate both seeds and pathogenic parasite eggs. Using wildlife cameras, we documented over 40 potentially susceptible vertebrate species in latrines and adjacent habitat. Latrine contact rates reflected background activity, diet preferences and disease risk. Disease‐tolerant raccoons and rats displayed significant site attraction, while susceptible birds and small mammals avoided these high‐risk sites. This suggests that parasites, like predators, might create a landscape of fear for vulnerable hosts. Such non‐consumptive parasite effects could alter disease transmission, population dynamics, and even ecosystem structure.

Fear of feces? Tradeoffs between disease risk and foraging drive animal activity around raccoon latrines

The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genus Neotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts.

Sara B. Weinstein

Papers

Independent origins of parasitism in Animalia.

Ecological and Evolutionary Consequences of Parasite Avoidance.

A landscape of disgust.

Fear of feces? Tradeoffs between disease risk and foraging drive animal activity around raccoon latrines

Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats ( Neotoma spp.)