Although parasites are increasingly recognized for their ecosystem roles, it is often assumed that free‐living organisms dominate animal biomass in most ecosystems and therefore provide the primary pathways for energy transfer. To examine the contributions of parasites to ecosystem energetics in freshwater streams, we quantified the standing biomass of trematodes and free‐living organisms at nine sites in three streams in western Oregon, USA. We then compared the rates of biomass flow from snails The trematode parasite community had the fifth highest dry biomass density among stream organisms (0.40 g/m2) and exceeded the combined biomass of aquatic insects. Only host snails (3.88 g/m2), sculpin (1.11 g/m2), trout (0.73 g/m2) and crayfish (0.43 g/m2) had a greater biomass. The parasite ‘extended phenotype’, consisting of trematode plus castrated host biomass, exceeded the individual biomass of every taxonomic group other than snails. The substantial parasite biomass stemmed from the high snail density and infection prevalence, and the large proportional mass of infected hosts that consisted of trematode tissue ( Estimates of yearly biomass transfer from snails into trematodes were slightly higher than the combined estimate of snail biomass transfer into the three vertebrate predators. Pacific giant salamanders accounted for 90% of the snail biomass consumed by predators. These results demonstrate that trematode parasites play underappreciated roles in the ecosystem energetics of some freshwater streams.
Non‐native freshwater snails can play important roles as consumers, hosts, and prey. Despite their potential ecological importance, global patterns in non‐native snail taxonomy, geography, and ecology have not been documented. Our objectives were to use a semi‐quantitative systematic review to describe non‐native freshwater snail global diversity, distribution, mechanisms of introduction, and interactions with natural enemies, including parasites and predators. Based on 506 relevant publications, we recorded 95 non‐native freshwater snail species from 16 families. Six taxonomic families, and pulmonate snails as a group, were over‐represented relative to the number of species expected by chance. Eight snail species represented 63% of the research records. A few snail taxa (15%) were widespread global invaders, reported from four or more continents, while most invasions were limited to a single continent. Australia and the Pacific Islands were the largest ‘sink’ for non‐native snails, with the greatest difference in the number of non‐native taxa relative to native taxa that had spread to other continents. Aquarium hobby sales were implicated as the most common mechanism of introduction (41% of species), followed by “hitchhiking” on aquatic vegetation, human consumption, use for biocontrol, transportation in canals, commercial shipping, and outdoor recreation. A search of internet sales posts indicated that four of the six over‐represented snail families were readily available for purchase online. Non‐native snails hosted parasites of wildlife, livestock, and human health importance, yet on average had 80% lower parasite richness in their non‐native compared to native range. At least 65 taxa were documented as consumers of non‐native snails, including native predators of conservation concern. These findings suggest that non‐native snails often are released from parasitism, but may commonly experience biotic resistance from predators. Our synthesis emphasizes the relatively high diversity of non‐native snails, but the disproportionate role of a few taxonomic groups in driving ecological, economic, and public health challenges. Moving forward, it will be important to limit new snail introductions through policy, education, and monitoring, particularly as the effective control of established snail invasions remains challenging in most ecosystems.
- NSF-PAR ID:
- 10445011
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Freshwater Biology
- Volume:
- 67
- Issue:
- 2
- ISSN:
- 0046-5070
- Page Range / eLocation ID:
- p. 227-239
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Juga plicifera into trematode parasites relative to aquatic vertebrate predators (sculpin, cutthroat trout and Pacific giant salamanders).M = 31% per snail). -
more » « less
Abstract Predation on parasites is a common interaction with multiple, concurrent outcomes. Free‐living stages of parasites can comprise a large portion of some predators' diets and may be important resources for population growth. Predation can also reduce the density of infectious agents in an ecosystem, with resultant decreases in infection rates. While predator–parasite interactions likely vary with parasite transmission strategy, few studies have examined how variation in transmission mode influences contact rates with predators and the associated changes in consumption risk.
To understand how transmission mode mediates predator–parasite interactions, we examined associations between an oligochaete predator
Chaetogaster limnaei that lives commensally on freshwater snails and nine trematode taxa that infect snails.Chaetogaster is hypothesized to consume active (i.e. mobile), free‐living stages of trematodes that infect snails (miracidia), but not the passive infectious stages (eggs); it could thus differentially affect transmission and infection prevalence of parasites, including those with medical or veterinary importance. Alternatively, when infection does occur,Chaetogaster can consume and respond numerically to free‐living trematode stages released from infected snails (cercariae). These two processes lead to contrasting predictions about whetherChaetogaster and trematode infection of snails correlate negatively (‘protective predation’) or positively (‘predator augmentation’).Here, we tested how parasite transmission mode affected
Chaetogaster –trematode relationships using data from 20,759 snails collected across 4 years from natural ponds in California. Based on generalized linear mixed modelling, snails with moreChaetogaster were less likely to be infected by trematodes that rely on active transmission. Conversely, infections by trematodes with passive infectious stages were positively associated with per‐snailChaetogaster abundance.Our results suggest that trematode transmission mode mediates the net outcome of predation on parasites. For trematodes with active infectious stages, predatory
Chaetogaster limited the risk of snail infection and its subsequent pathology (i.e. castration). For taxa with passive infectious stages, no such protective effect was observed. Rather, infected snails were associated with higherChaetogaster abundance, likely owing to the resource subsidy provided by cercariae. These findings highlight the ecological and epidemiological importance of predation on free‐living stages while underscoring the influence of parasite life history in shaping such interactions. -
more » « less
Abstract Disturbances are increasing in size and frequency with climate change, facilitating species that opportunistically exploit areas where habitat‐forming foundation species have been removed. Although it is well‐recognized that consumers, disease and weedy space‐holders can affect foundation species’ resistance to and recovery from disturbance, how predators influence their resilience is less clear.
In salt marshareas de‐vegetated by drought and intensive snail
Littoraria irrorata grazing (hereafter, ‘die‐offs’), we monitored bird use and experimentally manipulated bird and nekton access to the vegetated borders of die‐off mudflats across periods of both vegetation die‐off and regrowth to explore how these predators mediate the resilience of cordgrassSpartina alterniflora , the foundation species that structures US Atlantic coast salt marshes.Surveys revealed that birds, especially probers that agitate soils, forage year‐round for invertebrates in die‐off mudflats in our study area but not in adjacent vegetated areas.
During periods of die‐off, cordgrass borders accessible to bird and nekton predators retreated >3‐times slower and snail densities were halved, relative to predator exclusion cages. In predator‐accessible plots, slower border retreat corresponded to greater snail infection by a bird host‐dependent trematode parasite. During recovery, cordgrass borders revegetated more quickly, and snail densities declined faster over time in unmanipulated controls relative to predator exclusions.
Synthesis . These findings suggest that birds, through their transmission of parasites to snails, appear to act synergistically with snail‐consuming nekton to slow cordgrass loss after drought‐snail disturbances. Predator access also corresponds to faster cordgrass recovery as environmental conditions improve, although the mechanisms behind this need further investigation. Thus, predators that opportunistically forage within disturbances have the potential to suppress consumer impacts through multiple mechanisms, including consumption and disease transmission, thereby bolstering foundation species’ resilience and modulating whole ecosystem responses to climate change. -
more » « less
Abstract Agricultural expansion is predicted to increase agrochemical use two to fivefold by 2050 to meet food demand. Experimental evidence suggests that agrochemical pollution could increase snails that transmit schistosomiasis, a disease impacting 250 million people, yet most agrochemicals remain unexamined.
Here we experimentally created >100 natural wetland communities to quantify the relative effects of fertilizer, six insecticides (chlorpyrifos, terbufos, malathion, λ‐cyhalothrin, permethrin and esfenvalerate), and six herbicides (acetochlor, alachlor, metolachlor, atrazine, propazine and simazine) on two snail genera responsible for 90% of global schistosomiasis cases.
We identified four of six insecticides (terbufos, permethrin, chlorpyrifos and esfenvalerate) as high risk for increasing snail biomass by reducing snail predators. Hence, malathion and λ‐cyhalothrin might be useful for improving food production without increasing schistosomiasis. This top‐down effect of insecticides on predators was so strong that the effects of herbicides on schistosomiasis risk were masked in the presence of predators because there were so few snails. In the absence of snail predators, herbicide effects on snails were generally negative by reducing submerged vegetation
Hydrilla verticillata . The exception was that atrazine and acetochlor significantly increased the biomass of infected snails and total snails respectively.Like insecticides, fertilizer had strong positive effects on snail populations. Fertilizer increased both snail habitat (submerged vegetation) and snail food (periphyton), but of these two pathways, the increases in snail habitat resulted in greater snail population growth. Total snail biomass was positively associated with both infected snail biomass and parasite production and thus human infection risk.
Synthesis and applications . Our findings suggest that fertilizers and insecticides generally have consistently higher chances of increasing human schistosomiasis than herbicides in natural communities. Furthermore, our results highlight the need to identify other low risk insecticides, which might help reduce crop pests without increasing snails and thus risk of schistosomiasis. -
null (Ed.)Abstract Since 1955 snails of the Euglandina rosea species complex and Platydemus manokwari flatworms were widely introduced in attempted biological control of giant African snails ( Lissachatina fulica ) but have been implicated in the mass extinction of Pacific island snails. We review the histories of the 60 introductions and their impacts on L. fulica and native snails. Since 1993 there have been unofficial releases of Euglandina within island groups. Only three official P. manokwari releases took place, but new populations are being recorded at an increasing rate, probably because of accidental introduction. Claims that these predators controlled L. fulica cannot be substantiated; in some cases pest snail declines coincided with predator arrival but concomitant declines occurred elsewhere in the absence of the predator and the declines in some cases were only temporary. In the Hawaiian Islands, although there had been some earlier declines of native snails, the Euglandina impacts on native snails are clear with rapid decline of many endemic Hawaiian Achatinellinae following predator arrival. In the Society Islands, Partulidae tree snail populations remained stable until Euglandina introduction, when declines were extremely rapid with an exact correspondence between predator arrival and tree snail decline. Platydemus manokwari invasion coincides with native snail declines on some islands, notably the Ogasawara Islands of Japan, and its invasion of Florida has led to mass mortality of Liguus spp. tree snails. We conclude that Euglandina and P. manokwari are not effective biocontrol agents, but do have major negative effects on native snail faunas. These predatory snails and flatworms are generalist predators and as such are not suitable for biological control.more » « less
