Aquatic Biosystems

Background: One marbled crayfish, Marmorkrebs, Procambarus fallax f. virginalis (Hagen, 1870), was discovered in a natural ecosystem in Japan in 2006. Because Marmorkrebs are parthenogenetic, they could establish a population from only a single individual, and thus pose a risk for becoming established in Japan, as they have in other countries. There are two major reasons to be concerned about the possibility of Marmorkrebs establishing viable populations in Japan. First, Japan’s only endemic crayfish, Cambaroides japonicus (De Haan, 1841), lives throughout Hokkaido and is endangered. Introduced Marmorkrebs are potential competitors that could further threaten C. japonicus. Second, Marmorkrebs live in rice paddies in Madagascar and consume rice. Marmorkrebs populations could reduce rice yields in Japan. Results: We created five models in MaxEnt of the potential distribution of Marmorkrebs in Japan. All models showed eastern Honshu, Shikoku and Kyushu contain suitable habitats for Marmorkrebs. Hokkaido, the main habitat for C. japonicus, contained much less suitable habitat in most models, but is where the only Marmorkrebs in Japan to date was found. Conclusions: Marmorkrebs appear to be capable of establishing populations in Japan if introduced. They appear to pose minimal threat to C. japonicus, but may negatively affect rice production. Background In 2006, an unusual crayfish was collected in a river near Sapporo, and brought to the Sapporo Salmon Museum [1]. It had distinctive marbled colours, and all the offspring from this individual were later found to be female. This indicated that this crayfish was Marmorkrebs, a parthenogenetic [2, 3] crayfish that has been provisionally identified as Procambarus fallax f. virginalis (Hagen, 1870) [4]. (Here, we refer to the parthenogenetic form as “Marmorkrebs” and the sexual form as “P. fallax”). Marmorkrebs are unusual crayfish in two regards: they are the only known obligate parthenogenetic crayfish [2, 3], and the only known populations in natural ecosystems are the result of human introductions. Marmorkrebs have been introduced and established populations in Madagascar [5, 6] and Europe [7-10]. The discovery of Marmorkrebs in Hokkaido was the first well-documented case of an individual living in a natural ecosystem in Asia. Other reports of * Correspondence: [email protected] Department of Biology, The University of Texas-Pan American, Edinburg, TX, USA Full list of author information is available at the end of the article © 2012 Faulkes et al.; licensee BioMed Central Commons Attribution License (http://creativec reproduction in any medium, provided the or Marmorkrebs in Asia [11] have never been documented in the scientific literature or mainstream press. The most likely source of the Sapporo Marmorkrebs is a release or escape of a pet crayfish, as Marmorkrebs are widely circulated among aquarium hobbyists [12]. Marmorkrebs are parthenogenetic, and therefore a single female can initiate a stable population, resulting in an unwanted non-indigenous species. In Europe, single individual Marmorkrebs were discovered years before established populations were discovered [11, 13, 14]. Indeed, the delay was so long that it was questioned whether Marmorkrebs could establish populations in Europe [15]. This was a reasonable hypothesis, given that not all introduced species establish populations [16]. As it happened, Marmorkrebs have established populations in Germany [7], indicating that there was a “lag phase” [17] of several years between discovery of single individuals and establishment of populations. Thus, the discovery of the Sapporo Marmorkrebs may be a precursor to finding established populations of Marmorkrebs in Japan. We made quantitative models to assess the potential distribution of Marmorkrebs in Japan. There are at least two reasons to make such a threat assessment. First, Ltd. This is an Open Access article distributed under the terms of the Creative ommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and iginal work is properly cited. Faulkes et al. Aquatic Biosystems 2012, 8:13 Page 2 of 12 http://www.aquaticbiosystems.org/content/8/1/13 Japan has only one native crayfish species, Cambaroides japonicus (De Haan, 1841). The historic range of C. japonicus is Hokkaido and the northern regions of Honshu [18]. This species is endangered [19], due in part to the introduction of the North American crayfish species, Pacifastacus leniusculus [20-24]. The introduction of another exotic crayfish species could harm the remaining C. japonicus populations. Second, rice farming in Japan is economically important. Marmorkrebs have damaged rice paddies in Madagascar [14], although the extent of damage is not clear [5]. Marmorkrebs could become an agricultural pest in Japan if they become established. Thus, these models may help guide monitoring efforts, policy, and public information campaigns that could prevent further introductions or limit the spread. There are three common approaches to modeling the potential distribution of an exotic species: 1) extrapolate from the distribution of native populations only to the region of interest; 2) extrapolate from introduced populations in other regions to the region of interest; 3) extrapolate from a combination of native and introduced populations to the region of interest. Each of these methods has pros and cons, and it is not advisable to put too much weight on any single model [25]. The first, and probably the most common approach, for developing models of the potential distribution of an exotic species is to describe the native distribution of the species, and then extrapolate from the climatic variables associated with those regions to find other geographic areas that have similar climatic features [25, 26]. Strictly speaking, it is not possible to use this method with Marmorkrebs because there are no known populations in Table 1 Overview of MaxEnt models Trained on Sample size beta Threshold Procambarus fallax 37 1.0 MTSPS= 0.2 Procambarus fallax 37 1.5 MTP= 0.284 Marmorkrebs populations 23 1.0 MTSPS= 0.0 Marmorkrebs populations 23 1.5 MTP= 0.014 Marmorkrebs populations and Sapporo individual 24 1.0 MTSPS= 0.0 Marmorkrebs populations and Sapporo individual 24 1.5 MTP= 0.030 P. fallax and Marmorkrebs populations 58 1.0 MTSPS= 0.3 P. fallax and Marmorkrebs populations 58 1.5 MTP= 0.027 P. fallax, Marmorkrebs populations, and Sapporo individual 59 1.0 MTSPS= 0.3 P. fallax, Marmorkrebs populations, and Sapporo individual 59 1.5 MTP= 0.020 Training AUC is the AUC obtained in the 1-replicate run used for model selection a obtained in 10 runs that used a 30% of the presence points to calculate this statisti training AUC reduction were projected and test AUC calculated. MTSPS – minimum applicable – AICc cannot be calculated if the model have more parameters than occ the wild. We used the native distribution of P. fallax as a proxy for the native distribution of Marmorkrebs. We do so recognizing that, because the biotic conditions of each past introduction differ in overlap, the final fundamental niche space will vary depending on what dataset of presences is used to train the models [25]. As found in other studies of other species [27], invasive Marmorkrebs have a greater climatic range than wild P. fallax. There are many cases where parthenogens have quite distinct abilities and distributions than their sexual progenitors. This problem could be amplified by variation among clonal genotypes, which could be very distinct subsets of the range of abilities in the native sexual range. This has not been studied on Marmorkrebs yet, and using data from sexual P. fallax is a pragmatic approach. Other approaches to modeling potential distribution are to use established populations outside the native range, and a combination of the native and introduced populations. We use all three approaches (similar to [28]). We also created two additional models that included the location of the one Marmorkrebs individual discovered in Sapporo. These models including the Sapporo Marmorkrebs are speculative, because single individuals may not indicate that there is an established or even viable population [25]. Nevertheless, if it becomes apparent that there are established populations Marmorkrebs in Japan rather than single individuals, these models may help adjust the assessment of risk accordingly. Results According to the complexity of the models, measured as the number of parameters and lower AICc values (Table 1), and the visual inspection of response variables Parameters AICc score Training AUC Test AUC (30%) 84 12 874.2029424 0.9773 12 903.8337866 0.9764 0.9766 (0.0043) 33 22 not applicable 0.9844 18 760.5960693 0.9813 0.9823 (0.0146) 45 26 not applicable 0.9869 23 not applicable 0.9836 0.9723 (0.0212) 28 39 1829.92309 0.9673 27 1660.981878 0.9623 0.9595 (0.0119) 21 37 1882.800434 0.9640 24 1722.570932 0.9586 0.9537 (0.0148) nd MESS generation. Test AUC is the average AUC (and standard deviation) c; only models considered superior based on reduced complexity without training sensibility plus specificity; MTP – minimum training presence; not urrence points [29]. A P. fallax B Marmorkrebs C Marmorkrebs with Sapporo D P. fallax and