Cross-species amplification of microsatellite markers in the invasive spiny-cheek crayfish (Orconectes limosus): Assessment and application

The North American spiny-cheek crayfish,Orconectes limosus (Cambaridae), endangered in its native range, is a widespread invasive species in European waters and conservationally important carrier of crayfish plague. However, its population structure is poorly known, and no informative genetic markers for the species are available. We tested cross-species transfer of microsatellite loci to spiny-cheek crayfish from 5 other crayfish species. Variability of 10 successfully amplifying loci derived from 4 species was then tested in 60 individuals ofO. limosus originating from 3 natural populations: the river Danube at Bogyiszló in Hungary, a pond in Stary Klíčov, and the brook Černovicky, both in the Czech Republic. The allele number within the populations ranged from 4 to 10 alleles per locus, while heterozygosity levels varied from 0.650 to 0.900 forHo and from 0.660 to 0.890 forHe. No linkage disequilibrium and no null alleles were detected. The selected markers are useful for assessing population structure, intraspecific variation, and paternity studies in spiny-cheek crayfish.     

Threat of non-native crayfish introductions into Turkey: global lessons

Introductions of crayfish species from their home range to new environments have been carried out in many parts of the world. The most important introduced crayfish species are Procambarus clarkii, Pacifastacus leniusculus, Cherax destructor, C. quadricarinatus, Orconectes limosus, O. rusticus and Astacus leptodactylus. The environmental impact of crayfish introductions can be positive, negative or neutral. However, native crayfish populations in Europe have been negatively affected by introductions of non-indigenous crayfish species from America. Negative effects of non-native crayfish introductions included displacement of native crayfish species, transfer of disease (crayfish plague), consumption of fish eggs, reduction of fish stocks, consumption of large amounts of macrophytes, indirect and direct effects on other invertebrates and upsetting production in rice fields. As a result of non-native crayfish introductions, the natural harvest and crayfish industry in Europe have been severely affected. Large quantities of Turkish A. leptodactylus were harvested (approximately 7,000 tonnes annually) and exported to Europe before the crayfish plague was observed in these populations. The total harvest of A. leptodactylus in Turkey reduced dramatically to 320 in 1991 after the plague. Therefore, although Turkey currently has no known non-native crayfish species, there is a threat of non-native crayfish introduction in order to increase crayfish productions and subsequent harvest. The North American spiny-cheek crayfish, O. limosus, has been spreading quickly down the River Danube and could soon reach neighboring countries including Turkey. The North American signal crayfish, P. leniusculus is known from Greece and could be a threat to native stocks if it is introduced into Turkey for aquaculture. Additional threats may come from the release of other North American species, which are widely available through the aquarium trade. We conclude that the spread of non-native crayfish introductions throughout Turkey will increase local problems, because introductions of non-native crayfish in many parts of the world have been known to have caused important reductions in population density and numbers of native crayfish species. Furthermore, freshwater ecosystems may be altered by such introductions and the economic viability of native crayfish species fisheries could be severely reduced in Turkey.     

Temperature and prey density jointly influence trophic and non‐trophic interactions in multiple predator communities

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Scavenger-driven fish carcass decomposition and phosphorus recycling: Laboratory experiments with freshwater fish and crayfish

1. Fish carcass decomposition can generate fluxes of nutrients to the water column at levels comparable to other major nutrient sources. However, relatively little is known about the biological processes modulating fish decay or the rates at which carcass-bound nutrients are made available to the biota.
2. This study focused on quantifying scavenger-mediated phosphorus (P) recycling, because the availability of this essential element can regulate the trophic state of aquatic ecosystems.
3. To explore the role of some important macroscopic aquatic scavengers in P recycling, laboratory experiments were conducted where carcasses of two fish species (common bleak Alburnus alburnus; pumpkinseed Lepomis gibbosus) were offered to two size classes of black bullhead (Ameiurus melas) and two crustacean species (spiny-cheek crayfish Faxonius limosus; narrow-clawed crayfish Astacus leptodactylus).
4. Our results show that the black bullhead and the two crayfish species are highly efficient macroscopic decomposers as the P contents of scavenged carcasses were reduced at significantly higher rates compared to those of microbially decomposed (control) carcasses.
5. Pumpkinseed carcasses proved to be more resistant to rapid decomposition, as they typically lost lower proportions of their P content than bleak carcasses during the course of the experiments.
6. Scavengers sequestered a relatively large fraction (up to 33% in black bullhead and 36% in crayfish) of total carcass P in their bodies. This suggests that the consumer species used in this study can transfer/return considerable quantities of carcass-derived nutrients directly to higher trophic levels incorporated into their own tissues, and may serve as an additional, short-term sink of these nutrients.

     

An invasive species may be better than none: invasive signal and native noble crayfish have similar community effects

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Predicting the ecological impacts of a new freshwater invader: functional responses and prey selectivity of the ‘killer shrimp’, Dikerogammarus villosus,compared to the native Gammarus pulex

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Historical,human, and environmental drivers of genetic diversity in the red swamp crayfish (Procambarus clarkii) invading the Iberian Peninsula

1. Patterns of genetic diversity in invasive populations can be modulated by a range of factors acting at different stages of the invasion process, including the genetic composition of the source population(s), the introduction history (e.g. propagule pressure), the environmental suitability of recipient areas, and the features of secondary introductions.
2. The North American red swamp crayfish, Procambarus clarkii, is one of the most widely introduced freshwater species worldwide. It was legally introduced into Spain twice, near the city of Badajoz in 1973 and in the Guadalquivir marshes in 1974. Thereafter the species rapidly colonised almost the entire Iberian Peninsula.
3. We used seven nuclear microsatellites to describe the genetic diversity and structure of 28 locations distributed across the Iberian Peninsula and to explain the expansion process of the red swamp crayfish. Additionally, we analysed the relationship between environmental suitability and genetic diversity of the studied locations.
4. The red swamp crayfish had a clear spatial genetic structure in the Iberian Peninsula, probably determined by the two independent introduction events in the 1970s, which produced two main clusters separated spatially, one of which was dominant in Portugal and the other in Spain.
5. The human-mediated dispersal process seemed to have involved invasion hubs, hosting highly genetically diverse areas and acting as sources for subsequent introductions. Genetic diversity also tended to be higher in more suitable environments across the Iberian Peninsula .
6. Our results showed that the complex and human-mediated expansion of the red swamp crayfish in the Iberian Peninsula has involved several long- and short-distance movements and that both ecological and anthropogenic factors have shaped the genetic diversity patterns resulting from this invasion process. Early detection of potential invasion hubs may help to halt multiple short-distance translocations and thus the rapid expansion of highly prolific invasive species over non-native areas.

     

Differences in aggression,activity and boldness between native and introduced populations of an invasive crayfish

Aggressiveness, along with foraging voracity and boldness, are key behavioral mechanisms underlying the competitive displacement and invasion success of exotic species. However, do aggressiveness, voracity and boldness of the invader depend on the presence of an ecologically similar native competitor in the invaded community? We conducted four behavioral assays to compare aggression, foraging voracity, threat response and boldness to forage under predation risk of multiple populations of exotic signal crayfish Pacifastacus leniusculus across its native and invaded range with and without a native congener, the Shasta crayfish P. fortis. We predicted that signal crayfish from the invaded range and sympatric with a native congener (IRS) should be more aggressive to outcompete a close competitor than populations from the native range (NR) or invaded range and allopatric to a native congener (IRA). Furthermore, we predicted that IRS populations of signal crayfish should be more voracious, but less bold to forage under predation risk since native predators and prey likely possess appropriate behavioral responses to the invader. Contrary to our predictions, results indicated that IRA signal crayfish were more aggressive towards conspecifics and more voracious and active foragers, yet also bolder to forage under predation risk in comparison to NR and IRS populations, which did not differ in behavior. Higher aggression/voracity/boldness was positively correlated with prey consumption rates, and hence potential impacts on prey. We suggest that the positive correlations between aggression/voracity/boldness are the result of an overall aggression syndrome. Results of stream surveys indicated that IRA streams have significantly lower prey biomass than in IRS streams, which may drive invading signal crayfish to be more aggressive/voracious/bold to acquire resources to establish a population.     

Only the largest terrestrial carnivores increase their dietary breadth with increasing prey richness

1. Animals should adapt their foraging habits, changing their dietary breadth in response to variation in the richness and availability of food resources. Understanding how species modify their dietary breadth according to variation in resource richness would support predictions of their responses to environmental changes that alter prey communities.
2. We evaluated relationships between the dietary breadth of large terrestrial carnivores and the local richness of large prey (defined as the number of species). We tested alternative predictions suggested by ecological and evolutionary theories: with increasing prey richness, species would (1) show a more diverse diet, thus broadening their dietary breadth, or (2) narrow their dietary breadth, indicating specialisation on a smaller number of prey.
3. We collated data from 505 studies of the diets of 12 species of large terrestrial mammalian carnivores to model relationships between two indices of dietary breadth and local prey richness.
4. For the majority of species, we found no evidence for narrowing dietary breadth (i.e. increased specialisation) with increasing prey richness. Although the snow leopard and the dhole appeared to use a lower number of large prey species with increasing prey richness, larger sample sizes are needed to support this result.
5. With increasing prey richness, the five largest carnivores (puma Puma concolor, spotted hyaena Crocuta crocuta, jaguar Panthera onca, lion Panthera leo, and tiger Panthera tigris), plus the Eurasian lynx Lynx lynx and the grey wolf Canis lupus (which are usually top predators in the areas from which data were obtained), showed greater dietary breadth and/or used a greater number of large prey species (i.e. increased generalism).
6. We suggest that dominant large carnivores encounter little competition in expanding their dietary breadth with increasing prey richness; conversely, the dietary niche of subordinate large carnivores is limited by competition with larger, dominant predators. We suggest that, over evolutionary time, resource partitioning is more important in shaping the dietary niche of smaller, inferior competitors than the niche of dominant ones.

     

Crayfish invasion facilitates dispersal of plants and invertebrates by gulls

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Home-field advantage: native signal crayfish (Pacifastacus leniusculus) out consume newly introduced crayfishes for invasive Chinese mystery snail (Bellamya chinensis)

The introduction of non-indigenous plants, animals and pathogens is one of today’s most pressing environmental challenges. Freshwater ecologists are challenged to predict the potential consequences of species invasions because many ecosystems increasingly support novel assemblages of native and non-native species that are likely to interact in complex ways. In this study we evaluated how native signal crayfish (Pacifastacus leniusculus) and non-native red swamp crayfish (Procambarus clarkii) and northern crayfish (Orconectes virilis) utilize a novel prey resource: the non-native Chinese mystery snail (Bellamya chinensis). All species are widespread in the United States, as well as globally, and recent surveys have discovered them co-occurring in lakes of Washington State. A series of mesocosm experiments revealed that crayfish are able to consume B. chinensis, despite the snail’s large size, thick outer shell and trapdoor defense behaviour. Crayfish exhibited size-selective predation whereby consumption levels decreased with increasing snail size; a common pattern among decapod predators. Comparison of prey profitability curves—defined as the yield of food (weight of snail tissue) per second of feeding time (the time taken to crack the shell and consume the contents)—suggests that small and very large snails may represent the most profitable prey choice. By contrast, previous studies have reported the opposite pattern for crayfish consumption on thin-shelled snails. For all snail size classes, we found that native P. leniusculus and invasive O. virilis consumed greater numbers of snails than invasive P. clarkii. Moreover, P. leniusculus consistently handled and consumed snails at a faster pace compared to both invasive crayfishes across the range of snail sizes examined in our study. These results suggest not only that B. chinensis is a suitable food source for crayfish, but also that native P. leniusculus may ultimately out-consume invasive crayfishes for this new prey resource.     

Long-term variability and density dependence in Hudson River Dreissena populations

1. We used a 27-year record of Dreissena populations in the freshwater tidal Hudson River to describe interannual variation in population density, body size, and body condition; estimate long-term variation in recruitment, survivorship, and shell growth; and assess possible controls on the populations.
2. Dreissena populations in the Hudson have been highly variable, with interannual ranges of c. 100-fold in abundance and biomass, and 7-fold in mean body mass. This large interannual variation arises from both long-term trends and 2–5-year cycles.
3. Long-term trends include the 2008 appearance of the quagga mussel (Dreissena rostriformis), which still forms a small part (<10%) of the dreissenid community, and a decline in zebra mussel body size. The decline in body size was caused by a long-term decline in adult survivorship rather than a decline in rates of shell growth. We could detect no long-term trends in adult abundance or spread of Dreissena onto soft sediments in the Hudson.
4. We observed persistent, strong cycles in adult abundance and body size. These were driven by the appearance and decay of eight dominant year classes over the 27 years of our study, and were a result of temporal variation in recruitment rather than temporal variation in survivorship. The observed strongly irregular recruitment appears to arise from strong adult–larval interactions, and is consistent with previous simulation model results showing that interactions between adults and larvae can drive persistent cycling.
5. We found evidence that negative density dependence affects recruitment, somatic growth, and body condition of Dreissena in the Hudson. Warm summers may also cause high adult mortality.
6. We put our results into the context of a conceptual model of Dreissena population dynamics, and argue that neither the dynamics nor the controls of populations of these important invaders is known satisfactorily.

     

Phenotypic variability of rusty crayfish (Faxonius rusticus) at the leading edge of its riverine invasion

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Can the parthenogenetic marbled crayfish Marmorkrebs compete with other crayfish species in fights?

The parthenogenetic marbled crayfish, Marmorkrebs, has no known wild population, but has been introduced into natural ecosystems in two continents. Interactions with native crayfish, particularly through fighting, could affect the ecological impact of Marmorkrebs introductions. Marmorkrebs have been characterized anecdotally as having low levels of aggression, which could mitigate their potential to compete with native species. We isolated Marmorkrebs and Louisiana red swamp crayfish (Procambarus clarkii), then conducted size-matched intra and interspecific pairings. Marmorkrebs were as likely to win a fight as P. clarkii, although contests between P. clarkii and Marmorkrebs began significantly faster than contests between two Marmorkrebs. These results suggest that Marmorkrebs have the potential to compete with other species on the same level as P. clarkii, which is itself a highly successful introduced species around the world.     

Noise-induced reduction in the attack rate of a planktivorous freshwater fish revealed by functional response analysis

1. Anthropogenic noise can affect animals physically, physiologically, and behaviourally. Although individual responses to noise are well documented, the consequences in terms of community structure, species coexistence, and ecosystem functioning remain fairly unknown.
2. The impact of noise on predation has received a growing interest and alterations in trophic links are observed when animals shift from foraging to stress-related behaviours, are distracted by noise, or because of acoustic masking. However, the experimental procedures classically used to quantify predation do not inform on the potential demographic impact on prey.
3. We derived the relationship between resource use and availability (the functional response) for European minnows (Phoxinus phoxinus) feeding on dipteran larvae (Chaoborus sp.) under two noise conditions: ambient noise and ambient noise supplemented with motorboat noise. The shape and magnitude of the functional response are powerful indicators of population outcomes and predator–prey dynamics. We also recorded fish behaviour to explore some proximate determinants of altered predation.
4. For both noise conditions, fish displayed a saturating (type II) functional response whose shape depends on two parameters: attack rate and handling time. Boat noise did not affect handling time but significantly reduced attack rate, resulting in a functional response curve of the same height but with a less steep initial slope. Fish exhibited a stress-related response to noise including increased swimming distance, more social interactions, and altered spatial distribution.
5. Our study shows the usefulness of the functional response approach to study the ecological impacts of noise and illustrates how the behavioural responses of predators to noise can modify the demographic pressure on prey. It also suggests that prey availability might mediate the negative effect of noise on predation. Community outcomes are expected if the reduced consumption of the main food sources goes with the overconsumption of alternative food sources, changing the distribution pattern of interaction strengths. Predation release could also trigger a trophic cascade, propagating the effect of noise to lower trophic levels.

     

Predicting and testing functional responses: An example from a tardigrade–nematode system

Numerous studies have empirically measured consumer functional responses or theoretically developed response models, but whether these models can quantitatively predict observed data has hardly been tested. We perform such a test for the terrestrial predator–prey system Macrobiotus richtersi (Tardigrada)–Acrobeloides nanus (Nematoda). For two different size classes of A. nanus, we report a functional response as measured in the laboratory and quantitatively compare it to predictions of three models with different degrees of complexity: (1) the disc equation which does not include satiation effects; (2) the steady-state satiation (SSS) equation which assumes a constant level of predator satiation; and (3) the satiation model which accounts for prey depletion and increasing predator satiation over the course of the experiments. We parameterized these models with data that were measured independently of the functional response experiments. In both prey-size classes, the predictions of the satiation model matched the observations best, and the match came close to that of logistic regressions fitted to the observations. Thus, the parameterized satiation model seems to include the most important determinants of the functional response in our focal system. For understanding functional responses, we need more studies that compare data to independently derived model predictions.     

Native European eels as a potential biological control for invasive crayfish

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Biogeographic differences between native and non-native populations of crayfish alter species coexistence and trophic interactions in mesocosms

Biogeographical comparisons of native and non-native populations allow researchers to understand the degree to which traits contributing to invasion success are intrinsic or change during the invasion process. Here, we investigate whether traits underlying interspecific competition change following invasion and whether these alter the impacts of two crayfish congeners that have invaded into each other’s native ranges. Specifically, we compared native and non-native populations of rusty (Faxonius rusticus) and virile crayfish (F. virilis). We compared native and non-native populations of each species using laboratory assays to examine aggression and large mesocosms with the congeners in sympatry to examine growth and survival as well as impacts on lower trophic levels. We found that non-native virile crayfish were more aggressive in response to a threat than native virile crayfish and exhibited greater growth and survival in sympatry with rusty crayfish. These intraspecific differences were large enough to alter coexistence between species in the mesocosm experiment, which is consistent with patterns of coexistence between these species in the field. We did not observe differences in traits between native and non-native rusty crayfish, but rusty crayfish were consistently competitively dominant over virile crayfish in paired laboratory assays. Non-native populations of both species had greater impacts on lower trophic levels than native populations. Taken together, these findings provide new evidence that trait changes during invasions may enhance ecological impacts of invasive animals and their ability to compete with closely related native species.     

Effects of crayfish on leaf litter breakdown and shredder prey: are native and introduced species functionally redundant?

Recent increases in biological invasions frequency may have important consequences on native communities. However, functional redundancy between invasive and native species could reduce non-native species effects on native ecosystems. Despite this, even small differences in functional traits between these species may still have unpredictable effects on colonized ecosystems. Invasive crayfish, as ecosystem engineers, potentially have wide and complex effects on recipient ecosystems, even when replacing a native counterpart. We used laboratory microcosms to test whether native (Astacus astacus) and invasive crayfish species (Orconectes limosus, Pacifastacus leniusculus and Procambarus clarkii) are actually functionally redundant in their effects on prey/shredder density and leaf litter breakdown. Results show that crayfish strongly influenced macroinvertebrate numbers and leaf litter breakdown and indicate that differences in direct (prey and leaf litter consumption) and indirect (prey habitat use and leaf litter breakdown) effects between crayfish species do exist. While the replacement of A. astacus by O. limosus may have induced only minor changes in freshwater ecosystems, invasions by the larger and more aggressive P. clarkii and P. leniusculus will likely have strong effects on invaded ecosystem. Overall, there seems to be no functional redundancy between these four species and outcomes of crayfish invasion will likely be species specific.     

Seasonal movements of crayfish in a fluctuating wetland: implications for restoring wading bird populations

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