Exploiting chemical ecology to manage hyperparasitoids in biological control of arthropod pests

Insect hyperparasitoids are fourth trophic level organisms that commonly occur in terrestrial food webs, yet they are relatively understudied. These top‐carnivores can disrupt biological pest control by suppressing the populations of their parasitoid hosts, leading to pest outbreaks, especially in confined environments such as greenhouses where augmentative biological control is used. There is no effective eco‐friendly strategy that can be used to control hyperparasitoids. Recent advances in the chemical ecology of hyperparasitoid foraging behavior have opened opportunities for manipulating these top‐carnivores in such a way that biological pest control becomes more efficient. We propose various infochemical‐based strategies to manage hyperparasitoids. We suggest that a push‐pull strategy could be a promising approach to ‘push’ hyperparasitoids away from their parasitoid hosts and ‘pull’ them into traps. Additionally, we discuss how infochemicals can be used to develop innovative tools improving biological pest control (i) to restrict accessibility of resources (e.g. sugars and alternative hosts) to primary parasitoid only or (ii) to monitor hyperparasitoid presence in the crop for early detection. We also identify important missing information in order to control hyperparasitoids and outline what research is needed to reach this goal. Testing the efficacy of synthetic infochemicals in confined environments is a crucial step towards the implementation of chemical ecology‐based approaches targeting hyperparasitoids. © 2019 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.     

Effect of organic amendment amount on soil nematode community structure and metabolic footprints in soybean phase of a soybean-maize rotation on Mollisols

It has been well documented that organic amendment affects soil nematode community structure. However, little is known about the effect of organic amendment amount on soil nematodes. To assess the effect of the amount of organic amendments on soil nematode community structure and metabolic activity, the community composition, abundance, and metabolic footprints of soil nematodes were determined in a long-term field experiment with various amounts of organic amendment in Northeast China. Fertilization treatments included an unfertilized control (CK), chemical fertilizer without manure amendment (OM₀), manure applied at 7.5 Mg ha^-1 plus chemical fertilizer (OM₁), and manure applied at 22.5 Mg ha^-1 plus chemical fertilizer (OM₂). A total of 46 nematode genera were found. Treatments with the largest amount of organic amendment had the smallest number of plant parasite genera (5), but a largest number of dominant genera (7). Soil nematodes, bacterivores, and fungivores were the most abundant in OM₂, followed by OM₁, and the lowest in OM₀ and CK. Organic amendment increased the enrichment index (EI), and the large amount of organic amendment increased the metabolic footprints of bacterivore (Baf) and fungivore (Fuf) and enrichment footprint (Ef). The relationships between Baf (or Fuf) and the increases in soil organic carbon (ΔSOC) and total nitrogen (ΔTN) were stronger than those of bacterivore (or fungivore) abundance with ΔSOC and ΔTN, except for the relationship between bacterivore abundance and ΔSOC. The EI and Ef were positively correlated with ΔSOC and ΔTN. These findings suggest that the amount of organic amendment affects soil nematode activity and function at entry levels in soil food web, and that metabolic footprints of soil nematodes may be better indicators than their abundances in assessing their relationships with soil nutrients.     

Implications of piscine predator control on the federally listed fountain darter

One strategy for protecting the federally listed fountain darter, Etheostoma fonticola (Jordan & Gilbert), during low flow conditions is the removal of piscine carnivores [in this case, largemouth bass, Micropterus salmoides (Lacepède)]. However, headwater spring communities of the Comal and San Marcos rivers include another potential predator [red swamp crayfish, Procambarus clarkii (Girard)]. Removal of piscine carnivores could produce cascading effects by increasing crayfish consumption of benthic fish. The purpose of this study was to evaluate if piscine carnivore removal will lessen predatory pressure or induce a trophic cascade with crayfish increasing and causing declines in fountain darter. The numbers of fountain darter consumed were quantified among three predator treatments (red swamp crayfish only, largemouth bass only and red swamp crayfish and largemouth bass combined) and vegetation treatments (vegetated and non‐vegetated) at three temperature regimes (18, 22, 27°C). Vegetation had no effect on fountain darter predation. Among temperature trials, largemouth bass only and red swamp crayfish and largemouth bass combined consumed similar numbers of fountain darter, and red swamp crayfish only consumed the least numbers of fountain darter, except at 22°C. Largemouth bass did not consume more red swamp crayfish than fountain darter. Therefore, largemouth bass removal appears to be a viable option for reducing fountain darter predation during periods of low flow.     

Ontogenetic resource use and trophic dynamics of endangered juvenile Tachypleus tridentatus among diversified nursery habitats in the northern Beibu Gulf,China

Horseshoe crabs, the most well-known example of “living fossils”, are iconic and ecologically important macroinvertebrates in coastal and estuarine ecosystems. Their blood is a crucial resource for manufacturing Limulus or Tachypleus amebocyte lysate to detect bacterial endotoxins or fungal contamination in drug and medical devices. An enhanced understanding of their ecological roles and trophic interactions in the food webs is fundamental to facilitate resource management for the declining populations in Asia. Foraging information of the Asian species, however, is mainly derived from preliminary, scattered reports from a limited number of study locations. In this study, resource utilization, trophic niche dynamics, and trophic interaction of the juvenile tri-spine horseshoe crab, Tachypleus tridentatus (instars 1–12, approximately 0.5–8 years old) across ontogeny was assessed in diversified nursery habitats along the northern Beibu Gulf, China, using carbon and nitrogen stable isotopes. Our results suggest that: (i) T. tridentatus are ecological generalists given the vast range of carbon isotopic values and trophic niche width estimates exhibited between multiple instar groups; (ii) juvenile T. tridentatus across most habitat types predominantly assimilated energy from a variety of basal production sources in the food web, but primarily depended on sedimentary organic matter and seagrass resource pools; (iii) ontogenetic shifts in juvenile dietary proportions were evident, with decreased reliance on sedimentary organic matter, coupled with increased reliance on benthic macroinvertebrate grazers, detritivores, and omnivores with age; and (iv) nearly all juvenile instars occupied similar trophic positions in the food web with slight shifts in trophic position present with increasing size. Our findings indicate that resource availability and ontogenetic diet shifts strongly influence horseshoe crab trophic dynamics, and age should be accounted when formulating habitat conservation measures based on resource use for Asian horseshoe crabs.     

Diets of endangered silver chub (Macrhybopsis storeriana,Kirtland, 1844) in Lake Erie and implications for recovery

Silver chub (Macrhybopsis storeriana, Kirtland, 1844) is a native Cyprinid in Lake Erie, one of the Laurentian Great Lakes of North America. It is listed as endangered by the US state of New York and Canada, which has a recovery plan, and as special concern by the state of Michigan. Silver chub faces a potential threat to recovery from control efforts for invasive Grass carp (Ctenopharyngodon idella, Valenciennes 1844). Among the knowledge gaps for protection and restoration is current diet data. I describe the diet of silver chub from western Lake Erie in 2014, and I compare it to past studies to assess changes in diet through time. Silver chub captured in bottom trawls May–September 2014 were frozen in the field, and stomach contents were preserved in ethanol. Diet taxa were identified to the lowest practical taxonomic unit, then dried and weighed. Frequency of occurrence in silver chub diets was highest for Hexagenia spp. mayflies (79%). Dreissena spp. and Hexagenia spp. were both 41% of the diet by dry weight. Analysis of δ¹³C isotopes identified Hexagenia spp. as the primary source of carbon in silver chub. Compared to past studies, Dreissena spp. have mostly replaced Sphaeriidae and Gastropoda in silver chub diets. There also have been seasonal shifts in relative amounts of shelled organisms and Hexagenia spp. This study and past research suggest a functional link between silver chub and Hexagenia spp. abundance. Maintenance and recovery of silver chub may be dependent on maintaining Hexagenia spp. populations.     

Differing trophic niches of three French stygobionts and their implications for conservation of endemic stygofauna

1. Groundwater ecosystems represent the greatest proportion of unfrozen freshwater on Earth and harbour high numbers of rare taxa with restricted distributions. Stygofaunal abundance, species richness, and ecology play essential roles in groundwater ecosystem services and functioning, as well as providing an important contribution to global biodiversity. However, as global depletion and contamination of groundwater pose serious and often irreversible threats to stygofauna, more information is urgently needed about the ecology of rare groundwater species to guide effective strategies for their conservation or restoration.
2. In this study, analyses of carbon and nitrogen stable isotopes were used to compare and evaluate trophic niches and diets of a vulnerable stygobiont isopod, Gallasellus heilyi living in sympatry in French groundwater ecosystems with the isopod Caecosphaeroma burgundum and the amphipod Niphargus ladmiraulti.
3. Stable isotope results showed trophic niche partitioning among the three stygobiont species and indicated that G. heilyi and C. burgundum occupy the role of primary consumers and N. ladmiraulti that of predator. Moreover, although G. heilyi and C. burgundum were shown to rely on the same food sources, indicating similar diets, and their trophic niches did not overlap, suggesting trophic specialization.
4. The results suggest that detritus (i.e. decaying organic material) is an important food source for G. heilyi, and its availability could determine the survival of this endangered species. As a practical conservation measure for G. heilyi and the whole stygofauna community, we suggest reconnecting surface and subterranean ecosystems, as they probably were before natural sinks and many wells were filled up or closed.

     

Multi‐decadal climate and fishing predictors of abundance for U.S. South Atlantic coastal fishes and invertebrates

Abundance of marine stocks fluctuates in response to both internal processes (e.g., density dependence) and exogenous drivers, including the physical environment, fishing, and trophodynamic interactions. In the United States, research investigating ecosystem drivers has been focused in data‐rich systems, primarily in the North Atlantic and North Pacific. To develop a more holistic understanding of important ecosystem drivers in the Southeast U.S. continental shelf Large Marine Ecosystem, we applied generalized linear and dynamic linear modeling to investigate the effects of climate and fishing covariates on the relative abundance trends of 71 demersal fish and invertebrate species sampled by a coastal trawl survey during 1990–2013. For the assemblage as a whole, fishing effects predominated over climate effects. In particular, changes in trawling effort within the penaeid shrimp fishery governed abundance trends of bony fishes, invertebrates, and elasmobranchs, a likely result of temporal changes in bycatch mortality. Changes in trawling intensity induced changes in overall community composition and appear to have altered trophic interactions among particular species. Among climate indices investigated, the Pacific Decadal Oscillation and the Western Bermuda High Index were most prevalent in well‐supported dynamic linear models. Observed annual abundance trends were synchronous among some taxonomically related species, highlighting similar responses to exogenous influences based on life history. This study strengthens the foundation for generating hypotheses and advancing ecosystem‐based fisheries research within the region.     

Comparative ecologies of domestic and naturalised rainbow trout in northern Lake Huron

Northern Lake Huron (Ontario, Canada) supports the largest concentration of freshwater salmonid cage culture farms in Canada and receives inputs of domestic‐strain rainbow trout (Oncorhynchus mykiss) through escapement. We assessed the potential effects of these domestic fish on the naturalised rainbow trout of this ecosystem by comparing their respective ecologies. Mature adults were sampled from spawning tributaries, primarily in spring, and to a lesser extent in fall. Fish of domestic origin comprised ~80% of rainbow trout sampled from sites near cage culture facilities but <20% of rainbow trout sampled from more distant sites. Domestic adults in spawning condition (gametes free‐flowing) were present in the spawning tributaries in both spring and fall sampling seasons, whereas naturalised fish in spawning condition were only observed in the spring. Domestic adults were younger and smaller (in length), appeared to have shorter lifespan and had a higher male to female ratio compared with their naturalised counterparts. Growth rates (change in length with age) of naturalised and domestic females in the wild were similar, but domestic males grew more slowly than naturalised males. Domestic females also produced smaller eggs than naturalised females. Food web positions (inferred from δ¹³C and δ¹⁵N) of domestic and naturalised fish were very similar but varied more strongly with body size in the former. Domestic‐strain rainbow trout of cage culture origin can survive, grow and attempt to spawn in northern Lake Huron and have the potential to compete for food, mates and spawning habitat with naturalised rainbow trout.     

A comparison of changes in stable isotope ratios in the epidermal mucus and muscle tissue of slow‐growing adult catfish

Although stable isotope analysis is a powerful tool for determining diet, migration patterns and the structure of food webs in aquatic systems, the slow response of isotopic ratios in the widely used muscle tissue often hampers this approach, particularly in slow‐growing or adult fishes. We conducted a diet‐switch experiment to compare the changes in the stable carbon isotope ratio (δ¹³C values) in the epidermal mucus and muscle tissue of five‐year‐old catfish (Silurus asotus). The isotope ratios in noninvasively sampled mucus changed more rapidly than those in the muscle tissue. As isotopic change in mucus was relatively rapid, this technique can be used over a finer timescale than traditional isotopic analyses using the muscle tissue. The isotopic change half‐life in our experimental condition was 200 days, which would not be short enough for some research purposes. Examining mucus along with the muscle would enable food habits of slow‐growing fishes to be determined over different timescales. However, the rate of isotopic change in the mucus was negatively affected by the size of fish and was slower than the previously reported rates in juvenile steelhead. These findings suggest that mucus turnover rates need to be determined prior to the field data interpretation.     

Quantifying trophic interactions and niche sizes of juvenile fishes in an invaded riverine cyprinid fish community

Quantifying feeding interactions between nonindigenous and indigenous fishes in invaded fish communities is important for determining how introduced species integrate into native food webs. Here, the trophic interactions of invasive 0+ European barbel Barbus barbus (L.) and the three other principal 0+ fishes in the community, Squalius cephalus (L.), Leuciscus leuciscus (L.) and Phoxinus phoxinus (L.), were investigated in the River Teme, a River Severn tributary in Western England. B. barbus has been present in the River Teme for approximately 40 years. Analyses of stomach contents from samples collected from three sites between June and September 2015 revealed that, overall, fishes displayed a generalist feeding strategy, with most prey having low frequency of selection. Relationships of diet composition versus body length and gape height were species‐specific, with increasing dietary specialisms apparent as the 0+ fishes increased in length and gape height. The trophic niche size of invasive B. barbus was always significantly smaller than S. cephalus and L. leuciscus and was significantly smaller than P. phoxinus at two sites. This was primarily due to differences in the functional morphology of the fishes; 0+ B. barbus were generally restricted to foraging on the benthos, whereas the other fishes were able to forage on prey present throughout the water column. Nevertheless, the invasive B. barbus were exploiting very similar prey items to populations in their native range, suggesting these invaders were strongly pre‐adapted to the River Teme and this arguably facilitated their establishment and invasion.