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.     

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.     

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

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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.     

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.     

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.