Information use by an Invading Species: Do Invaders Respond More to Alarm Odors than Native Species?

Two species of crayfish were tested in the laboratory to evaluate the hypothesis that successful invaders use a broader range of chemical information than do displaced native species. The invasive species Orconectes rusticus reduced responses to food odors just as strongly when heterospecific (O. propinquus, O. virilis) alarm odors were introduced with food odors as they did when conspecific alarm odors were introduced at the same time as food odors. Individuals of the displaced native species, O. propinquus, did not reduce feeding responses as strongly when O. virilis alarm odor was introduced as with conspecific alarm odor or O. rusticus alarm odor. These results are consistent with the hypothesis that successful invaders use a wider range of information about their environment than do displaced native species.     

The smell of danger: chemical recognition of fish predators by the invasive crayfish Procambarus clarkii

1. Since avoiding predation can compromise animal fitness, prey are expected to respond to different predator species with an intensity appropriate to the level of risk. In fresh waters, the threat of predation is typically assessed by chemical cues, in particular by odours released by either injured/disturbed conspecifics (conspecific alarm odour) or predators (predator odours). Here, we used the most widely distributed crayfish in the world, the invasive North American Procambarus clarkii, to investigate the relative effectiveness of odours emitted by fish predators compared with conspecific alarm odour. We also tested whether P. clarkii is able to discriminate between fish predators of which it has ‘experience’ (either recent, via introduction to the same water body, or old, by sharing a native range), as well as between fish predators that pose low or high risk. 2. The study was carried out on introduced populations of P. clarkii from two sites, characterised by different fish assemblages: the Malewa River (a tributary of Lake Naivasha, Kenya) and Lake Trasimeno (Italy). Laboratory experiments consisted of three sequential phases (‘water’, ‘food’ and ‘smell’ phases) and five treatments. Treatments differed in the odour presented during the smell phase, i.e. no odour (plain water) and odours from either injured conspecifics or three fish species per site. Crayfish from the Malewa River population were confronted with the odours of largemouth bass (Micropterus salmoides), common carp (Cyprinus carpio) and tilapia (Tilapia zillii) (all introduced to Lake Naivasha but absent from the Malewa River), and those from the Lake Trasimeno population with the odours of the introduced largemouth bass and carp and the native chub (Squalius cephalus). Largemouth bass is the only predator that imposes a high risk to crayfish, and it also shares its native range with P. clarkii. We analysed the time spent by crayfish feeding, in locomotion and in adopting a raised or lowered posture. A reduction in the time spent feeding and in locomotion, and an increase in the time spent in the lowered posture were considered to indicate alarm. 3. Crayfish from both populations responded with a more pronounced reduction in feeding to conspecific alarm odour rather than to predator odours. Crayfish from the Malewa River reacted with the same intensity to the odours of the three fish species tested, whereas, in Lake Trasimeno, the odour of largemouth bass was significantly more threatening than the odours of the other two species. 4. Procambarus clarkii seems to perceive a general fish odour that alerts it to possible predation risk without the need of either a direct recent experience or via sharing a common native range. However, where they coexist with fish, crayfish become able to distinguish among species, adapting the intensity of their response to the effective risk. Our results confirm the relatively high learning capacity of P. clarkii reported in previous studies and suggest the existence of mechanisms that make predator recognition particularly efficient in this extraordinarily successful invader.     

The Effects of Starvation on Crayfish Responses to Alarm Odor

The effect of starvation on responses to alarm odor was tested with individuals of an invasive and a native species of crayfish. I predicted that chemical predator cues would inhibit feeding less in starving than well-fed animals, and that this decrease would be stronger in a native compared with an invasive species. Individuals were exposed to food odor and then alarm odor after 3 and 10 d of starvation. The inhibition of food-related behavior patterns was similar on the 2 d of testing for individuals of the invasive species, Orconectes rusticus. Individuals of O. virilis showed a significant reduction in the effects of alarm odor detection on day 10 compared with day 3 of starvation. The lack of a change in responses to alarm odors between days of testing by individuals of O. rusticus may be because they are more responsive to alarm odors than individuals of O. virilis. This behavioral difference could contribute to the successful range extension of O. rusticus.     

Austropotamobius pallipes reduction vs. Procambarus clarkii spreading: Management implications

One of the main threats to native European crayfish is the spread of alien crayfish species that are immune carriers of the detrimental crayfish plague Aphanomyces astaci. In this study we analyzed both at a regional and at a local scale factors determining native and alien crayfish distribution in an area where the species Procambarus clarkii is currently spreading. We aim to understand which management strategies could prevent the extinction of native populations. We sampled 81 waterbodies in Lombardy (NW Italy) to assess the Austropotamobius pallipes complex and alien crayfish occurrence; we also monitored the only first order stream in our study area that we found to be currently inhabited by A. pallipes upstream and by P. clarkii downstream. A. pallipes generally occurred in small brooks, near the spring, and was linked to low periphyton abundance, while P. clarkii occurred in sites at lower altitudes, far from the spring area, mainly in lentic waterbodies with large widths; this allochthonous species was positively related to periphyton abundance. Our monitoring showed that physical barriers such as dams may prevent P. clarkii dispersal upstream. Our results confirm that A. pallipes and P. clarkii have different ecological requirements and show that, at least during the first years of invasion, P. clarkii spreading involves lowland or downstream altered sites. We suggest the need for management strategies maximizing connectivity among native populations, to avoid isolation, and promoting the separation of native populations from those of P. clarkii.     

Influence of conspecific and heterospecific aggregation cues and alarm odors on shelter choice by syntopic spiny lobsters

In spiny lobsters, conspecific scents ("aggregation cues") may mediate gregarious diurnal sheltering, but scents from injured conspecifics ("alarm odors") may elicit avoidance behavior. In laboratory experiments, individuals of two coexisting species, Panulirus guttatus (a reef-obligate) and P. argus (a temporary reef-dweller), significantly chose shelters emanating conspecific aggregation cues and responded randomly to shelters emanating heterospecific aggregation cues. However, despite evidence that the two species perceived each other's alarm odors to a similar extent, P. guttatus responded randomly to shelters emanating either conspecific or heterospecific alarm odors, whereas P. argus significantly avoided both. This differential influence of alarm odors likely reflects interspecific differences in life history, sociality, and behavior. The less social, reef-obligate P. guttatus lobsters forage close to their reef dens, into which they retract deeply upon perception of risk. This cryptic behavior may offset the need to avoid conspecific (and heterospecific) alarm odors. In contrast, avoidance of conspecific alarm odors by P. argus is consistent with its ontogenetic habitat shifts and greater sociality. Furthermore, because reef-dwelling P. argus lobsters forage across open areas away from the reef, an ability to avoid alarm odors from P. guttatus upon returning to their reef dens may increase their fitness.     

Causes and consequences of crayfish extinction: Stream connectivity,habitat changes,alien species and ecosystem services

相似文献   

AFLP-PCR and RAPD-PCR evidences of the transmission of the pathogen Aphanomyces astaci (Oomycetes) to wild populations of European crayfish from the invasive crayfish species, Procambarus clarkii

Aphanomyces astaci (Oomycetes) is responsible for the crayfish plague disease. This species is endemic of North America and five genotypes have been described using RAPD-PCR. The red swamp crayfish, Procambarus clarkii, is one of the most widely spread North American species and invasive in the world. However, no outbreaks on its specific genotype, i.e., genotype D, have ever been described in nature. We investigated three major series of crayfish plague outbreaks in indigenous crayfish populations of Austropotamobius pallipes, located in the areas of influence of P. clarkii. All samples collected tested positive for A. astaci using a rnDNA ITS-PCR test. We also performed an AFLP-PCR analysis on 19 isolates, and found that all isolates belong to genotype D. These isolates exhibited similar properties, i.e., adaptation to warm temperatures. We demonstrate, for the first time, the transmission of A. astaci genotype D to indigenous European populations of crayfish, and confirm that the properties of adaptation to warm water temperatures seem to be a specific character of genotype D. The results of this work emphasize once more the need of controlling invasive species and its trade, since they can carry harmful pathogens with specific adaptations or increased virulence in new environments.     

Prevalence of the Crayfish Plague Pathogen Aphanomyces astaci in Populations of the Signal Crayfish Pacifastacus leniusculus in France: Evaluating the Threat to Native Crayfish

Aphanomyces astaci, the crayfish plague pathogen, first appeared in Europe in the mid-19^th century and is still responsible for mass mortalities of native European crayfish. The spread of this parasite across the continent is especially facilitated by invasive North American crayfish species that serve as its reservoir. In France, multiple cases of native crayfish mortalities have been suggested to be connected with the presence of the signal crayfish Pacifastacus leniusculus, which is highly abundant in the country. It shares similar habitats as the native white-clawed crayfish Austropotamobius pallipes and, when infected, the signal crayfish might therefore easily transmit the pathogen to the native species. We investigated the prevalence of A. astaci in French signal crayfish populations to evaluate the danger they represent to local populations of native crayfish. Over 500 individuals of Pacifastacus leniusculus from 45 French populations were analysed, plus several additional individuals of other non-indigenous crayfish species Orconectes limosus, O. immunis and Procambarus clarkii. Altogether, 20% of analysed signal crayfish tested positive for Aphanomyces astaci, and the pathogen was detected in more than half of the studied populations. Local prevalence varied significantly, ranging from 0% up to 80%, but wide confidence intervals suggest that the number of populations infected by A. astaci may be even higher than our results show. Analysis of several individuals of other introduced species revealed infections among two of these, O. immunis and P. clarkii. Our results confirm that the widespread signal crayfish serves as a key reservoir of Aphanomyces astaci in France and therefore represents a serious danger to native crayfish species, especially the white-clawed crayfish. The prevalence in other non-indigenous crayfish should also be investigated as they likely contribute to pathogen transmission in the country.     

The Decline of the Endangered Populations of the Native Freshwater Crayfish (Austropotamobius pallipes) in Southern Spain: It is Possible to Avoid Extinction?

The southeastern mountains of Spain represent the southernmost limit of the genus Austropotamobius and the species A. pallipes (Lereboullet). The taxonomic position of this isolated crayfish in southern Spain is not clear, being genetically close to A. italicus, but morphologically distinct. A severe decline occurred during the 1980s, especially due to expansion of the alien species Procambarus clarkii, a North American freshwater crayfish and a vector of the aphanomycosis disease. In order to design a strategy for native crayfish conservation, recent trends in native crayfish populations, influence of isolation and habitat variables on their survival and possibilities for their recovery through restocking were studied. A decline in populations was observed between 1991 and 2002 (from 26 to 14 populations), and a total extinction could be predicted within the next 13 years. Two well-defined periods of rapid extinction rates were detected, 1991–1994 (1.25 populations/year) and 1999–2002 (1.50 populations/year). Main causes of extinction for these two periods were invasion by P. clarkii and mortality by unknown causes, respectively. The isolation variables had some positive effects on survival of populations but these cannot offer a sufficient guarantee, since several cases of extinction can be affected by a large component of stochastic factors, including random catastrophes. On the other hand, survival trials and restocking experiments showed that it was possible to recover lost habitats, when P. clarkii was absent and environmental conditions were good. It is concluded that it is possible to avoid extinction of the native crayfish populations; however, the conservation strategies must be based on an urgent stocking/restocking program.     

Competition and parasitism in the native White Clawed Crayfish Austropotamobius pallipes and the invasive Signal Crayfish Pacifastacus leniusculus in the UK

Many crayfish species have been introduced to novel habitats worldwide, often threatening extinction of native species. Here we investigate competitive interactions and parasite infections in the native Austropotamobius pallipes and the invasive Pacifastacus leniusculus from single and mixed species populations in the UK. We found A. pallipes individuals to be significantly smaller in mixed compared to single species populations; conversely P. leniusculus individuals were larger in mixed than in single species populations. Our data provide no support for reproductive interference as a mechanism of competitive displacement and instead suggest competitive exclusion of A. pallipes from refuges by P. leniusculus leading to differential predation. We screened 52 P. leniusculus and 12 A. pallipes for microsporidian infection using PCR. We present the first molecular confirmation of Thelohania contejeani in the native A. pallipes; in addition, we provide the first evidence for T. contejeani in the invasive P. leniusculus. Three novel parasite sequences were also isolated from P. leniusculus with an overall prevalence of microsporidian infection of 38% within this species; we discuss the identity of and the similarity between these three novel sequences. We also screened a subset of fifteen P. leniusculus and three A. pallipes for Aphanomyces astaci, the causative agent of crayfish plague and for the protistan crayfish parasite Psorospermium haeckeli. We found no evidence for infection by either agent in any of the crayfish screened. The high prevalence of microsporidian parasites and occurrence of shared T. contejeani infection lead us to propose that future studies should consider the impact of these parasites on native and invasive host fitness and their potential effects upon the dynamics of native-invader systems.     

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.     

The North American crayfish <Emphasis Type="Italic">Procambarus clarkii</Emphasis> is the carrier of the oomycete <Emphasis Type="Italic">Aphanomyces astaci</Emphasis> in Italy

Aphanomyces astaci (Saprolegniales, Oomycetes) is classified among the 100 world’s worst invasive species. This species is endemic to North America and has been introduced into Europe by imports of their hosts, the North American crayfish species. As a consequence, extensive mass mortalities involved several populations of the European crayfish. Here, we checked its occurrence in four Italian populations of Procambarus clarkii, the most widespread alien crayfish in Italy. Digital image analyses and image processing techniques were used to select micro-melanized areas in the subabdominal cuticle of 2–10 crayfish per population. All the selected areas tested positive for A. astaci ITS nrDNA specific primers; moreover, the obtained sequences clearly corresponded to A. astaci, thus revealing that P. clarkii is an active carrier of this oomycete in Italy. Decisions are to be urgently made to control the spread of both P. clarkii and A. astaci for the conservation of the indigenous crayfish biodiversity.     

Ethological Isolation,Sexual Behavior and Pheromones in the Fasciatus Species Group of the Lizard Genus Eumeces

Ethological isolation was found among North American members of the fasciatus species group of Eumeces. Ethological isolation was investigated by staging a series of interspecific and intraspecific heterosexual encounters. No male E. laticeps or E. fasciatus courted heterospecific females. In both species, males courted and copulated with conspecific females in a significantly higher frequency of trials than with heterospecific females. However, male E. inexpectatus courted females of all three species, courting conspecific females and female E. laticeps at similar frequencies, but female E. fasciatus at a significantly lower frequency. No females of any of the three species were sexually receptive to heterospecific males, but forced copulation occurred in two of nine courtships of female E. fasciatus by male E. inexpectatus. Thus, ethological isolation in the fasciatus group appears to be complete with the possible exception of occasional forced copulation between male E. inexpectatus and female E. fasciatus. Preliminary evidence on the role of chemical stimuli in maintaining ethological isolation was obtained from experiments involving interspecific transfers of female odors. Male E. inexpectatus courted female E. fasciatus labelled with the odor of female E. inexpectatus in a significantly greater proportion of trials than they courted such females lacking the conspecific female odor. In a similar experiment, male E. fasciatus did not court female E. inexpectatus even if the females bore odors of female fasciatus.     

Movement, dispersal and refuge use of co-occurring introduced and native crayfish

1. Dispersal and habitat use are key elements in determining impacts of introduced species. We examined if an invasive crayfish species showed a different pattern of movement, dispersal and refuge use to that of a species that it displaces. 2. Fifteen adults of the introduced American signal crayfish, Pacifastacus leniusculus and 20 adult native white‐clawed crayfish Austropotamobius pallipes were radiotagged in an area of river where in 2003 they co‐occurred and the spatial behaviour and habitat use of the two species were examined. Subsequent surveys at the study site in 2005 recorded no A. pallipes and the density of P. leniusculus had increased. 3. Clear differences in the spatial behaviour of the two species were found. The median distance moved per day by signal crayfish was over twice that of white‐clawed crayfish, and dispersal from release locations was higher in signal crayfish. A similar range of refuges with a high degree of overlap was used by both species suggesting that the potential for competitive interaction between the two species exists. 4. The greater movement and dispersal by signal crayfish recorded here supports the hypothesis that invaders are better dispersers than the species that they displace. In addition, movements by signal crayfish may allow them to make better use of patchy resources than white‐clawed crayfish and this, coupled with similar microhabitat use, may contribute to the observed replacement.     

Early assessment of the impact of alien species: differential consequences of an invasive crayfish on adult and larval amphibians

Aim Early assessment of the impact of invasive alien species is crucial to set up timely management, but often the impact is evident when it is too late for action. We evaluated relationships between the alien crayfish, Procambarus clarkii, the distribution of native amphibians, and the abundance of their larvae. We assessed whether considering measures of reproductive success provide a more prompt measure of impact than considering just species distribution. Location One hundred and twenty‐five wetlands in Northern Italy, in an area recently invaded by P. clarkii. Methods We surveyed wetlands to assess the presence of breeding activity of amphibians and the distribution of P. clarkii. We measured the abundance of amphibian larvae before metamorphosis through pipe sampling. We built models analysing the relationships between amphibian and crayfish distribution, while taking into account spatial autocorrelation and environmental features. Analyses were performed at both the species level (generalized linear models and spatial eigenvector mapping) and community level (constrained redundancy analysis). Results In terms of breeding site distribution, only two amphibians (Lissotriton vulgaris and Hyla intermedia) were negatively associated with P. clarkii, while the relationships between other the species and P. clarkii were positive or not significant. However, larval abundance for all amphibian species was negatively associated with the alien crayfish. Analyses performed at community and single species levels yielded consistent results. Main conclusions Procambarus clarkii impacts amphibians through different processes. Newts probably avoid invaded wetlands for breeding. Other species attempt breeding in wetlands with crayfish, but suffer very low success. Considering distribution data alone would not provide a correct picture of the impact of this alien species; measures of reproductive success may allow a more accurate assessment of the impact.     

Geographic expansion of the invasive red crayfish <Emphasis Type="Italic">Procambarus clarkii</Emphasis> (Girard, 1852) (Crustacea: Decapoda) in Mexico

The red crayfish Procambarus clarkii, which is native to southcentral USA and northeastern Mexico, has been successfully introduced into several countries around the world. This study documents the geographic expansion of the exotic red crayfish in Mexico and discusses the consequence of a greater propagation of this species in Mexican inland waters. New state records of this crayfish in the Baja California peninsula and in the states of Durango and Sinaloa indicate its progressive dispersion. The propagation of P. clarkii in Mexico has been caused mainly by human introduction, but it is also facilitated because of the species’ tolerance to an ample range of environmental conditions. Because of the invasive capability of P. clarkii, we suspect that this exotic species is competing for habitat and food with native freshwater shrimp of the genus Macrobrachium in many sites of northern Mexico.     

Comparison of trophic function between the globally invasive crayfishes <Emphasis Type="Italic">Pacifastacus leniusculus</Emphasis> and <Emphasis Type="Italic">Procambarus clarkii</Emphasis>

Impacts of invasive species may manifest most strongly if these organisms are highly distinct functionally from the native species they often replace. Yet, should we expect functional differences between native and invasive species of generalist organisms like freshwater crayfish? Some existing evidence has pointed to native and invasive crayfish species as ecologically equivalent. We contribute to this literature by comparing the trophic niches of the globally invasive crayfishes Pacifastacus leniusculus and Procambarus clarkii, by applying carbon and nitrogen stable isotope analyses to replicated allopatric (alone) and sympatric (together) lake populations in western Washington State, USA, where P. clarkii has been recently introduced and P. leniusculus is presumed native. Our study corrected for potential inherent differences in lake food webs as a consequence of lake abiotic or biotic characteristics using random effects in linear mixed effects models. We found that although overall trophic niche size or area of these species was not significantly different, P. leniusculus was significantly higher in trophic position than P. clarkii when also accounting for the effects of body size, sex, and lakes as random effects. This pattern of increased trophic position of P. leniusculus over P. clarkii was conserved over time in one sympatric lake for which we had data over multiple years. Cumulatively, our findings point to trophic differences between the globally cosmopolitan crayfishes P. leniusculus and P. clarkii, particularly when accounting for the ways that ecosystem context can affect food web structure of communities and the trophic resources available to these consumers.     

Using avatar species to model the potential distribution of emerging invaders

Aim Anticipating the potential distributions of emerging invasive species is complicated by the tendency for species distribution models to perform better when both native and invasive range data are available for model development. If invasive range data are lacking, species models are liable to under‐estimate distributions for emerging invaders, particularly for species that are not at equilibrium with their native range environment due to historical factors, dispersal limitation and/or ecological interactions. We demonstrate the potential to use well‐quantified niche shifts from established ‘avatar’ (i.e. the remote or virtual manifestation of an entity) invaders to develop plausible distributions for data‐poor emerging invaders contingent on niche shifts of similar magnitude or character. Location Global. Methods Using the globally invasive crayfishes Pacifastacus leniusculus and Procambarus clarkii as our avatar invaders, we quantify how niche position, size and structure differs between native and total ranges using Mahalanobis distance (a measure of multivariate similarity) and the climate predictors of annual minimum and maximum air temperature. We then generalize patterns of niche shift from these species to the emerging crayfish invader Cherax quadricarinatus. Results Some patterns of niche shifts were similar for Pacifastacus leniusculus and Procambarus clarkii, but niche shifts were of considerably greater magnitude for P. clarkii. When a native range model for C. quadricarinatus was modified with generalized niche shifts similar to Pacifastacus leniusculus and Procambarus clarkii, the potential global distribution for this species increased considerably, including many areas not identified by the native range model. Main conclusions We illustrate the potential to use avatar invaders to provide cautionary, niche shift‐assuming species distribution models for emerging invaders. Many theoretical and applied implications of the avatar species concept require additional investigation, including the development of frameworks to select appropriate avatar species and evaluate the performance of avatar‐derived models for emerging invaders. Despite these research needs, we believe this concept will have considerable utility for predicting vulnerability to invasion by data‐poor species; this is a critical management need because shifting pathways of introduction and climate change will produce many novel, emerging invasive species in the future.