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Triggers affecting crayfish burrowing behaviour

Triggers affecting crayfish burrowing behaviour Aquat Ecol https://doi.org/10.1007/s10452-023-10057-3 Edwin T. H. M. Peeters  · Robin de Vries · Jesper Elzinga · Mercédesz Ludányi · Robbert van Himbeeck · Ivo Roessink Received: 8 May 2023 / Accepted: 29 August 2023 © The Author(s) 2023 Abstract Surface water inhabiting crayfish are burrowing was investigated under standardized labo- well-known for the impact on their surroundings. ratory conditions to reveal differences among species This impact has been related to loss of biodiversity and their sex. All studied species occur in the Neth- and deteriorating water quality for invasive crayfish. erlands and were the native Astacus astacus (Lin- Crayfish dig burrows for various reasons like lack of naeus, 1758), the Eurasian Pontastacus leptodactylus natural shelters, avoiding an upcoming drought, or (Eschscholtz, 1823) and the invasive North American high crayfish density and this may lead to increased Faxonius virilis (Hagen, 1870), F. limosus (Rafin- sediment transport and accelerated bank instability. esque 1817), Pacifastacus leniusculus (Dana, 1852), All crayfish are considered to have burrowing capa- Procambarus acutus (Girard 1852), and P. clarkii bility, but not all species have been observed burrow- (Girard, 1852). As burrowing triggers were evalu- ing. Studies comparing this behaviour among differ - ated presence of shelter, increased light intensity, ent species in standardized ways are scarce. Crayfish increased water temperature, and increased crayfish density. Results showed species-specific and some- times sex-specific differences in burrowing behaviour Handling editor: Télesphore Sime-Ngando. among crayfish. The response to burrowing triggers Supplementary Information The online version was also species-specific and no two species reacted contains supplementary material available at https:// doi. identical to all triggers. Absence of shelter was a org/ 10. 1007/ s10452- 023- 10057-3. E. T. H. M. Peeters (*) · R. de Vries · J. Elzinga · Present Address: M. Ludányi · R. van Himbeeck  M. Ludányi  Chairgroup Aquatic Ecology and Water Quality BioAqua Pro Ltd., Debrecen, Hungary Management, Wageningen University, Wageningen, The Netherlands Present Address: e-mail: edwin.peeters@wur.nl R. van Himbeeck  Laboratory of Nematology, Wageningen University, Present Address: Wageningen, The Netherlands R. de Vries  Wageningen, The Netherlands I. Roessink  Environmental Risk Assessment Group, Wageningen Present Address: Environmental Research, Wageningen, The Netherlands J. Elzinga  Environmental Engineering Department, Van Oordt Dredging and Marine Contractors, Rotterdam, The Netherlands Vol.: (0123456789) 1 3 Aquat Ecol strong driver to burrow for A. astacus, F. limosus and 2016; Roessink et  al. 2017). Furthermore, the bur- F. virilis, while increased light intensity triggered rows they dig may lead to increased sediment trans- burrowing behaviour in P. leptodactylus, P. acutus port in streams (Sanders et  al. 2021) and may cause and P. clarkii and lowered activity of F. limosus. Bur- or accelerate river bank instability and erosion (Arce rowing behaviour of P. clarkii was mostly influenced and Diéguez-Uribeondo 2015; Faller et  al. 2016; by increased water temperature. Significant differ - Harvey et  al. 2019), collapse of delimiting banks ences between females and males were observed for in rice fields (Arce and Diéguez-Uribeondo 2015), P. leptodactylus, P. leniusculus and P. acutus in the and increase the risk of compromised riverbanks in shelter, increased density and increased water tem- peatland areas (Lemmers et  al. 2021). Although all perature treatment, respectively. Understanding the freshwater crayfish species have the ability to burrow triggers that invoke burrowing may help managing (Hobbs 1981; Crandall and De Grave 2017; Florey populations of these invasive species. and Moore 2019), there is also a number of crayfish species that live in permanent water which burrow- Keywords Density · Invasive species · Light ing may be limited (Berrill and Chenoweth 1982). intensity · Shelter · Water temperature These observations have been made under different field conditions and studies that compare this burrow - ing capacity among species under similar conditions Introduction are very scarce but see e.g. Burras et  al. (1995) and Kouba et al. (2016). Crayfish that inhabit open waters (tertiary and sec- It is generally accepted that burrows function as a ondary burrowers) are well-known for their impact means to withstand environmental extremes (e.g. high on the surrounding biotic and abiotic environment temperatures) and as a protection against predators, (Hobbs 1981). Due to this profound effect on their especially during sensitive life history phases (Barba- environment they are regarded as ecosystem engi- resi et al. 2004; Stoeckel et al. 2011). But what triggers neers (Statzner et  al. 2003; Albertson and Daniels burrowing behaviour in the different crayfish species? 2018). Through their feeding and foraging behav- Although burrowing might be a direct result of envi- iour, crayfish can have a great negative impact on ronmental stress (Correia and Ferreira 1995), triggers benthic macroinvertebrate communities (Correia and for this behaviour seem rather unpredictable (Barbaresi Anastácio 2008; Souty-Grosset et  al. 2016). This and Gherardi 2006). An important reason for crayfish may result in less biodiverse communities in places to excavate is seeking shelter as burrowing appeared to where they occur compared to places where they are be inversely related to the availability of natural shel- absent. The impact of invasive crayfish on the native ters present (Flint 1975; Berrill and Chenoweth 1982; macroinvertebrate community can be either compa- Ilhéu et  al. 2003). Burrowing activities can be up to rable to (Weber and Traunspurger 2017) or greater five times higher when there is a lack of protection but (Nystrom et al. 1999) than the impact native crayfish depends of the bottom structure (Flint 1975). Crayfish have. Since almost all invasive species are carriers leave shelters for feeding during the night because risk of the crayfish plague, their presence obviously limit of predation is lower, and this risk increases parallel the distribution of native species in Europe (Tilmans to increasing light intensities (Flint 1975; Ranta and et  al. 2014; Souty-Grosset et  al. 2016; Mojžišová Lindström 2010). The observed withdrawal of crayfish et  al. 2020, 2022). Crayfish species may also nega- towards their burrows when light intensities increased tively affect emergent, floating or submerged plants (Suzuki et al. 1985; Fernández-De-Miguel and Aréch- by grazing (Nystrom and Strand 1996) and, especially iga 1992) supports the notion that burrowing and light the loss of submerged plants may lead to increased intensity might be correlated. Increasing light intensity turbidity of the water (Roessink et  al. 2017). The can also act as an early warning signal for an upcoming relatively substantial individual body size in combi- drought that can have a detrimental effect on crayfish nation with their behaviour (walking, fighting, for - populations (McClain 2013; Kouba et  al. 2016). Sur- aging) and eventually high population densities may vival of crayfish outside of water is species dependent lead to physical disturbance of the sediment that (Reynolds et  al. 2012), and a link has been observed negatively affects water quality (Souty-Grosset et  al. between drought and burrowing activities (Correia and Vol:. (1234567890) 1 3 Aquat Ecol Ferreira 1995; Barbaresi et al. 2004). Increase in water bath (see pictures of Online Resource 1) to ensure a temperature is another signal that can be associated stable and comparable water temperature (18–20 °C). with dry periods (Boulton 2003) and higher water tem- Each crate had an additional PVC wall installed peratures stimulate the activity and metabolism of cray- to mimic a bank and to create a visual wall for the fish (Flint 1975). Furthermore, biological factors like crayfish. Two openings in this wall provided access crayfish density may affect burrow use with a higher to a PVC pipe (Ø 5.8  cm) with one filled with 25 occupancy rate of burrows at higher P. clarkii densities blue foam blocks of 3–4  cm to provide burrowing (Ranta and Lindström 2010). Although no relationship opportunities, and the other pipe open to provide a seems to exist between burrow density and P. clarkii shelter or closed off, depending on the treatment. population size (Ilhéu et al. 2003), the number of active Copper-free tap water was used to fill the crates burrows has been positively correlated with the popu- until ten centimetres below the top (48  L), minimiz- lation size (Arce and Diéguez-Uribeondo 2015). Bur- ing escapes. Aeration via a tube with an air stone rowing behaviour has also been linked to the reproduc- was provided in each crate to maintain stable dis- tive cycle (Romaire and Lutz 1989; Holdich and Black solved oxygen levels, while a shade cloth above the 2007) with earlier burrowing activity in the season creates prevented stress caused by too high artificial by female P. leniusculus (Stanton 2004), larger and light intensity as shown in the pictures of Online deeper burrows by female P. clarkii (Guo et  al. 2020) Resource 1. Light intensity under the shade cloth but −2 −1 and, especially females with eggs retreating in burrows above the crates averaged around 85  µmol  m  s −2 −1 (Hasiotis 1995).(range 74–100 µmol  m  s ). A day-night regime of Currently, there are several invasive crayfish spe- 10–14 h was applied. cies with well-established populations in the Neth- Each treatment (Table  1) was tested for three suc- erlands while only one species is native (Lemmers cessive days. Twelve crates per run were available and et al. 2021). This offers the opportunity to study bur - in each run six males and six females were deployed. rowing behaviour in a standardized way among dif- Depending on the availability of animals and time, in ferent crayfish species. The prime aim of the present principle two runs were performed per species and study was to investigate crayfish burrowing behav - treatment, giving twelve observations per sex for one iour and reveal possible differences among seven treatment. All runs for a species were usually per- crayfish species and their sex. The second aim was formed within a period of two months. To minimize to identify which triggers invoke this behaviour. In human impact on crayfish behaviour, the room with a laboratory experimental set-up, four possible trig- the water bath was only accessed by the observers gers, namely the presence of shelter, increased light to daily check the well-being of all individuals dur- intensity, increased water temperature, and increased ing a run. After each run, all materials were cleaned crayfish density were evaluated for burrowing behav - with fresh water and the crates were refilled with iour in the native species Astacus astacus (Linnaeus, new water to remove any odour from previous cray- 1758), the Eurasian species Pontastacus leptodactylus fish. In case a crayfish removed at least three blocks (Eschscholtz, 1823) non-native to the Netherlands, (out of 25) from the pipe, this was regarded as bur- and the invasive North American species Faxonius rowing behaviour. In a number of cases, crayfish tried virilis (Hagen, 1870), Faxonius limosus (Rafinesque, to escape the crate and when this occurred this was 1817), Pacifastacus leniusculus (Dana, 1852), Pro- recorded as an escape response. The first response cambarus acutus (Girard, 1852), and Procambarus (digging or escaping) determined the result for that clarkii (Girard, 1852). crayfish for that treatment. Treatments Materials and methods Five different treatments were tested (Table  1). In the General set-up burrowing experiment control treatment, the one PVC pipe in the crates was covered with a PVC plate while the other pipe was Twelve plastic crates of 60 × 40 × 30 filled with the blue foam blocks (size approximately (length × width × height) cm were placed in a water 1.5 × 1.5 × 1.5  cm). Crayfish were allowed to burrow Vol.: (0123456789) 1 3 Aquat Ecol Table 1 Overview of tested treatments. All treatments had a standard water temperature (18–20 °C) and a standard light intensity −2 −1 (85 μmol  m  s ) and one crayfish per crate unless stated otherwise Treatment Description Schematic representation Control One pipe filled with blue foam and the other pipe blocked by a PVC plate Shelter As the Control treatment, but with one additional empty pipe representing a place to shelter Increased light intensity As the Control treatment but light intensity above the crate was −2 −1 increased in two days to an average of 200–280 µmol  m  s after 1 run-in day Increased water temperature As the control treatment but temperature of the water in the crate was increased in two day with 3 °C per day (6 °C in total) after 1 run-in day Increased crayfish density As the control treatment but a second crayfish was introduced in the tank. At the start of the experiment, the crayfish were sepa- rated from each other for 10 min with a perspex T-structure Drawing crayfish by Pearson Scott Foresman for nearly three days (66 h including, two nights). In intensity. After this pre-treatment night, the treat- the shelter treatment, the pipe with foam was avail- ment started by increasing the light intensity above −2 −1 able and from the other pipe the cover was removed the crates during daytime to 200–80 µmol  m  s by to provide a shelter possibility. The increased light adapting the emitted intensity of the artificial lamps intensity treatment started with one day (one night) to the required level. Crayfish were again offered to of acclimatization to the conditions that correspond burrow for three days (two nights). The increased to the control treatment with only the pipe filled with water temperature treatment also started with one day foam available. All crayfish that showed a response (one night) of acclimatization to the control treatment within this one day were removed from the treatment conditions with again only the pipe filled with foam because the response was not triggered by higher light available. Crayfish that showed a response within this Vol:. (1234567890) 1 3 Aquat Ecol one day were removed from the treatment because the sex and length of carapace were determined. Due to response was not triggered by higher water tempera- logistical issues, not all treatments were tested for ture. After the pre-treatment, water temperature was all species by sex combinations. Control and shelter gradually increased with 3 °C per day until it reached treatment were performed for all species but both 26 °C by increasing the temperature of the water bath. sexes of F. virilis could not be tested for increased For the density treatment, crayfish were individually light intensity and increased water temperature and placed in buckets 24  h before the start of the test to both sexes of F. limosus, P. acutus and P. clarkii were ensure that they were free from odours of other cray- not tested for density effects. Each crayfish specimen fish in their housing tank. Thereafter, they were trans- was in principle used in all tests and were given at ferred into the crates under similar conditions as the least seven days between two trials to recover. control treatment. In each container two individuals from the same sex and species were introduced and a divider separated the individuals for the first ten min- Data analysis utes to let them get used to each other’s smell, with- out seeing each other. The divider was removed and Both the water temperature and light intensity treat- both crayfish were free to burrow. ment had an one day run-in period using the standard conditions from the control experiment. Specimens Crayfish that showed a response during this first day and night were removed from the treatment. As a consequence, Seven crayfish species were tested over the years a lower number of replicates for that treatment was (Table  2). Most invasive crayfish were wild-caught available for statistical testing and for some species by either local fisherman or by the staff. Faxonius the number of observations became lower than a-pri- limosus and P. clarkii originated from Hardinxveld- ori anticipated. Density treatment was always per- Giessendam (the Netherlands), F. virilis from the formed at the end of the series of tests. This was done floodplains of the river Waal near Boven-Leeuwen to avoid damages that may arise when specimens (the Netherlands), and P. leniusculus from the Oude fight with each other, so we ensured that all other Leij in Tilburg (the Netherlands). Procambarus acu- tested treatments were performed with intact animals. tus originated from a culture (Harald Groβ, Edelkrebs The number of times that burrowing, escaping and und Fischzucht, DE) and P. leptodactylus frome a no responses occurred were determined per treat- commercial supplier (Koidreams, Valburg, NL) while ment and per species and sex. Fisher’s exact tests Astacus astacus came from an own culture. in SPSS (Field 2013) were applied to test whether Prior to the experiment, crayfish were housed the observed responses (burrowing, escaping or no separately to avoid fights and injuries. Three pellets response) of a single species (females and males of Trouvit (Skretting, a Nutreco company) were fed separately and taken together) in a specific treat- to each crayfish twice a week. Each individual got an ment significantly differed from the control treat- unique number written with Tipp-Ex on the carapace ment. Adjusted standardized residuals were evaluated for individual recognition during the experiment and to discover which observed response deviated from Table 2 Overview of the Species English name Origin Period of testing n seven species, their origin, period of testing (month Astacus astacus Noble crayfish Europe 06–2015 24 and year), and available Pontastacus leptodactylus Narrow-clawed crayfish Eurasia 05–2015 23 number of specimens (n) Pacifastacus leniusculus Signal crayfish North America 09–2016 till 50 for the experiment 01–2017 Faxonius limosus Spiny-cheek crayfish North America 04–2013 23 Faxonius virilis Virile crayfish North America 04–2016 24 Procambarus acutus White river crayfish North America 04–2013 21 Procambarus clarkii Red swamp crayfish North America 04–2013 22 Vol.: (0123456789) 1 3 Aquat Ecol Vol:. (1234567890) 1 3 Aquat Ecol Fig. 1 Relative distribution of responses for all treatments for ◂ shelter, increased light intensity, and increased the tested seven species separated by sex. No bar means not water temperature treatment, all specimen showed tested, except for male A. astacus, that responded already in no response and the difference with the control the acclimatization period of the increased light intensity and treatment was significant (Table  4) except for the increased water temperature treatment. F = females, M = males increased water temperature treatment due to the lower number of observations in this treatment. the expectation. A p value ≤ 0.05 indicated a signifi- These differences were mainly due to changes in the cant difference while a value between 0.05 and 0.10 behaviour of the females. was regarded as indicating a trend. Fisher’s exact test Faxonius virilis actively burrowed in the control was also used to statistically evaluate the differences treatment (Fig.  1) and offering shelter significantly between sexes per species in the different treatments (Table  4) reduced the number of burrowing speci- and to evaluate differences between species. mens. In the increased crayfish density treatment, significantly more specimens tried to escape the experimental setting. Results Approximately half of P. leniusculus specimens burrowed in the control treatment (Fig.  1) and the Figure 1 shows a summary of the obtained results and shelter and increased light intensity treatment did the raw data counts can be found in Online Resource not result in significant changes in behaviour. In the 2. increased water temperature and increased crayfish density treatments, one third of the males and none Sex-specific response behaviour of the females burrowed and the difference of the latter with the control treatment were significant In a number of cases, the response of females to a (Table 4). treatment differed significantly from males (Fig.  1, Around 40–50% of P. leptodactylus burrowed Table  3). Significantly (p ≤ 0.05) less P. leptodac- in the control treatment (Fig.  1) and in the shelter tylus males burrowed in the shelter treatment, less treatment only males burrowed significantly less P. acutus males in the increased water temperature (Table 4). In the increased light intensity treatment, treatment and more P. leniusculus males burrowed in significantly more specimens burrowed which was the increased crayfish density treatment. There was due to the males. No significant differences were a trend (0.05 < p ≤ 0.10) in more P. acutus females observed due to the increased water temperature or showing no response in the shelter treatment and increased crayfish density. less P. leniusculus females showing a response in the Roughly 10% of P. acutus specimens burrowed in increased water temperature treatment. the control treatment (Fig.  1) and this did not sig- nificantly (Table  4) change in the shelter treatment Species-specific response behaviour despite the trend in response between females and males. In the increased light intensity and increased Astacus astacus was an active burrower (95% of the water temperature treatment, more specimens specimen) in the control treatment (Fig.  1), and bur- showed a response but this was not significant. rowing activity was significantly (Table  4) lower in Less than 5% of the P. clarkii specimens bur- the shelter treatment. All males responded during the rowed in the control treatment (Fig. 1) and a similar acclimatization period for both the increased light pattern was observed for the shelter treatment which intensity and increased water temperature treatment. was not significantly (Table  4) different from the Increased light intensity resulted in a trend with fewer control treatment. Both increased light intensity and females burrowing compared to the control treatment. increased water temperature significantly reduced Increased water temperature did not lead to significant the number of specimens without a response in changes in females. Increased crayfish density signifi- favour of more burrowing or males trying to escape. cantly lowered burrowing activity in this species. A quarter of the specimens of F. limosus bur- rowed in the control treatment (Fig.  1). In the Vol.: (0123456789) 1 3 Aquat Ecol Table 3 Results of Fisher’s exact test (Chi-square, p value, degree of freedom, total observations) to evaluate the significance of sex per species Treatment Fisher’s Test A. astacus P. leptodactylus P. leniusculus F. limosus F. virilis P. acutus P. clarkii Control χ2 1.043 0.436 1.387 4.346 1.846 1.143 1.210 p 1.000 0.407 0.531 0.104 0.482 0.803 1.000 df 1 1 2 2 1 2 2 n 24 23 50 23 24 21 22 Shelter χ2 1.423 8.224 1.938 Constant 0.938 4.090 Constant p 0.796 0.006 0.580 1.000 0.095 df 2 1 2 2 2 n 21 24 26 24 24 15 14 Increased light availability χ2 N.D 2.250 1.869 Constant N.A 1.044 0.938 p 0.333 0.608 0.807 1.000 df 1 2 2 2 n 9 15 21 20 15 Increased water temperature χ2 N.D 1.400 4.550 Constant N.A 8.507 3.497 p 0.280 0.070 0.009 0.257 df 1 2 2 2 n 14 13 9 22 14 Increased crayfish density χ2 0.133 0.105 4.800 N.A 2.630 N.A N.A p 1.000 1.000 0.047 0.315 df 1 1 1 2 n 26 22 24 16 N.A.: not tested at all, N.D.: no data available because all specimens from one sex escaped during the acclimatization period, Con- stant: no variability in response due to the exact same response by females and males Significant (p ≤ 0.05) differences between females and males are in bold and italic and trends (0.05 < p ≤ 0.10) in bold only Differences in response behaviour among species virilis specimens showed this escape behaviour in the density experiment. Both Procambarus species were The species tested in the treatments showed signifi- triggered to burrow by increased light intensity and cantly different behaviour (Table  5). Astacus asta- especially increased water temperature. The increased cus and F. virilis burrowed significantly more in the water temperature treatment resulted in the highest control treatment while only a small fraction of F. response of P. clarkii to stimuli. Increased light inten- limosus and both Procambarus species burrowed. A sity also triggered male P. leptodactylus to dig. The similar pattern was observed in the shelter treatment. increased crayfish density treatment triggered F. viri- In the increased light and increased water temperature lis to escape, a response that was not observed for the treatment, P. leptodactylus burried more frequently other species. than the other tested species F. limosus, P. lenius- culus and both Procambarus species. Pacifastacus leniusculus burrowed less than P. leptodactylus, F. Discussion virilis and A. astacus while F. virilis more frequently escaped. In this laboratory study, crayfish were placed in an Roughly 50% of A. astacus and P. leptodactylus artificial environment with one pipe filled with pieces dug in all treatments (Fig. 1) which is in contrast with of foam to study their burrowing behaviour. Pipes of the lack of burrowing in a number of treatments for F. comparable diameter have been successfully used as limosus, P. acutus and P. clarkii. Procambarus acu- shelters in other experiments with tertiary crayfish tus and P. clarkii and male P. leniusculus more fre- (Gherardi and Daniels 2003; Payette and McGaw quently escaped than the other species. Half of the F. 2003; Stanton 2004; Barbaresi and Gherardi 2006) Vol:. (1234567890) 1 3 Aquat Ecol Table 4 Results of Fisher’s exact test (Chi-square, p value, degree of freedom, number of observations) to evaluate the significance of observed difference in behaviour between the treatment and control Species Shelter Increased light intensity Increased water tempera- Increased crayfish density ture χ2 p df n χ2 p df n χ2 p df n χ2 p df n A. astacus 7.887 0.009 2 45 11.435 < 0.001 1 50 F 5.972 0.021 2 21 4.500 0.098 1 18 2.976 0.217 2 24 8.000 0.007 1 24 M 2.403 0.158 1 24 N.D N.D 3.914 0.060 1 26 P. leptodactylus 0.260 0.552 1 47 5.420 0.024 1 32 0.149 0.481 1 37 0.237 0.428 1 45 F 1.623 0.200 1 24 0.268 0.554 1 15 0.220 0.485 1 22 0.686 0.340 1 24 M 1.168 0.275 1 23 6.491 0.017 1 17 0.170 0.593 1 15 0.029 0.608 1 21 P. leniusculus 2.213 0.379 2 76 1.740 0.401 2 65 4.877 0.071 2 63 9.058 0.007 2 74 F 3.184 0.216 2 39 0.907 0.797 2 33 8.018 0.013 2 33 13.282 < 0.001 2 38 M 1.616 0.594 2 37 2.932 0.268 2 32 1.607 0.590 2 30 0.864 0.814 2 36 F. limosus 8.562 0.004 2 47 7.586 0.014 2 44 3.216 0.188 2 32 N.A F 7.738 0.014 2 24 7.181 0.023 2 23 4.129 0.150 2 18 N.A M 1.140 0.478 1 23 1.339 0.524 1 21 0.294 0.786 1 14 N.A F. virilis 10.127 0.003 2 48 N.A N.A 12.788 < 0.001 2 40 F 6.471 0.018 1 22 N.A N.A 9.330 0.005 1 19 M 4.246 0.097 2 26 N.A N.A 3.179 0.236 2 21 P. acutus 0.862 0.854 2 36 4.210 0.127 2 41 0.729 0.824 2 43 N.A F 2.742 0.405 2 23 2.229 0.432 2 22 3.207 0.244 2 23 N.A M 0.325 0.510 1 13 2.701 0.404 2 19 0.586 0.392 2 20 N.A P. clarkii 1.262 1.000 2 36 7.553 0.014 2 37 11.920 0.001 2 36 N.A F 1.023 1.000 2 20 3.024 0.366 2 23 5.927 0.025 2 21 N.A M Constant 5.091 0.055 1 14 7.645 0.007 2 15 N.A F females, M males, N.A. not tested at all, N.D. no data available because all specimens from one sex escaped during the acclimatiza- tion period constant: exactly the same response in treatment and control Treatments that significantly (p ≤ 0.05) deviated from control are in bold and italic and trends (0.05 < p ≤ 0.10) in bold only and match sizes of occupied burrows in field obser - present study might be underestimated for the spring/ vations (Souty-Grosset et  al. 2014). The number of early season. burrows dug by crayfish has been related to type and Burrowing behaviour has also been linked to the composition of the sediment (Stanton 2004; Emery- reproductive cycle (Romaire and Lutz 1989; Hold- Butcher et  al. 2023). The foam used in this study ich and Black 2007) and especially to females with does not resemble natural sediments at all, and may eggs retreating in burrows (Hasiotis 1995). To avoid therefore have affected the burrowing behaviour of bias in the results due to a few gravid females, these the tested species. However, all species showed to be specimens were excluded from the experiment. The able to remove the foam from the pipe and occupy the different runs for each species were performed within pipe in at least one of the treatments and, therefore, a relatively short period of time and by that excluding the general set-up is regarded suitable as a means to seasonal variation. The advantage of this approach study burrowing behaviour in a standardized way. is that significant differences among treatments are The various species were tested in spring/early sum- indeed due to the applied triggers and thus shed light mer in different years, except for P. leniusculus that on how each species responds to the triggers applied. was tested in autumn/early winter. Since activity of P. The responses, however, may change over the seasons leniusculus shows a seasonal cycle with low activity and repeating the experiments in other seasons may in winter (Flint 1977), their burrowing activity in the reveal the consistency in response to the triggers. Vol.: (0123456789) 1 3 Aquat Ecol Vol:. (1234567890) 1 3 Table 5 Results of Fisher’s exact tests to evaluate differences in response among species to the treatments Treatment Fisher’s exact test Behaviour Species χ2 p df n A. astacus P. leptodactylus P. leniusculus F. limosus F. virilis P. acutus P. clarkii Control 86.836 < 0.001 12 187 Burrow 5.1 -0.4 0.2 -2.2 4.7 −3.7 −4.3 Escape − 1.2 − 1.2 0.2 − 0.2 − 1.2 4 − 0.2 No Response − 4.6 0.9 − 0.3 2.3 − 4.1 1.9 4.3 Shelter 45.319 < 0.001 12 148 Burrow 3.4 1.8 0 − 3.5 2.3 − 2.1 − 2.6 Escape 0.2 − 1.1 1 − 1.1 0 1.9 − 0.8 No Response − 3.4 − 1.3 − 0.5 3.9 − 2.2 1.2 2.9 Increased light intensity 29.734 < 0.001 8 80 Burrow 3.8 0.1 − 3.7 0.3 0.7 Escape N.T − 0.8 1.3 − 1.4 N.T 0.8 0.1 No Response − 3.3 − 0.7 4.2 − 0.7 − 0.7 Increased water temperature 16.48 0.017 8 72 Burrow 2.2 − 1 − 1.9 − 1 1.6 Escape N.T − 1.6 − 0.6 − 1.2 N.T 1.7 1.1 No Response − 1 1.3 2.6 − 0.2 − 2.2 Increased crayfish density 37.024 < 0.001 6 88 Burrow 1.9 − 0.3 − 2.6 1 Escape − 1.8 − 1.6 − 1.7 N.T 5.8 N.T N.T No Response − 0.9 1.1 3.4 − 4.2 Test results (Chi-square, p value, degree of freedom, total observations) are given as well as the standardized residuals. Significant standardized residuals are in bold and italic. Positive values indicate more frequently observed and negative values less frequently observed N.T. species not tested Aquat Ecol Crayfish use refuge and burrows to be pro- females in burrow activity prior to mating and Ber- tected against predators, to withstand environmental rill and Chenoweth (1982) also found no differences extremes or for reproduction (Hobbs 1981; Barbaresi between sexes. On the other hand, the study of Guo et al. 2004; Stoeckel et al. 2011). Excavating burrows et  al. (2020) indicated that there were differences by crayfish seem to be inversely linked to the avail- between female and male P. clarkii in shelter use also ability of natural shelters present (Berrill and Che- outside the reproductive period. In the present study, noweth 1982; Ilhéu et  al. 2003). When no shelter in which no gravid females were used, most treatment was present in our experiment, certain species show and species combinations did not show sex-specific active burrowing behaviour (A. astacus, F. virilis, P. responses and thus supports the lack of differences in leptodactylus), while others show hardly any bur- burrowing behaviour between males and females. rowing activity (P. clarkii, male F. limosus), limited Crayfish use natural refuges besides burrows to burrowing activity (female F. limosus, P. leniusculus) seek shelter and the presence of natural shelters seem or only limited escape behaviour (P. acutus). In per- to reduce burrowing activity (Flint 1975; Ilhéu et  al. manent water with similar environmental laboratory 2003; Groza et  al. 2016). The observations in the conditions, the examined crayfish species thus differ present study showed that the presence of a shelter in their burrowing response. Our laboratory findings indeed reduced burrowing behaviour in A. astacus, F. therefore, support the field observations that among limosus, and F. virilis. Interestingly, the presence or crayfish that live in open water some species burrow absence of a shelter did not lead to a change in their and others not depending on the prevailing conditions behaviour of P. leniusculus, P. leptodactylus, P. acu- (Berrill and Chenoweth 1982). This burrowing capa- tus and P. clarkii. Remarkably, for F. limosus, lack of bility seems, however, to be flexible since P. lenius- shelter was the only environmental stressor that trig- culus, which is considered a non-burrowing species, gered burrowing behaviour. According to the results heavily burrowed outside its native range in the banks of the present study, the response to shelter availabil- of a river in the UK (Guan 1994) and also showed ity is likely to be species-specific. burrowing behaviour in our study. Similarly, Kaestner Crayfish species vary in their ability to survive out (1991) and Statzner et al. (2000) mention that F. limo- of water (Reynolds et al. 2012; Kouba et al. 2016) and sus does not burrow while other sources e.g. Holdich one way to deal with desiccation is excavating bur- and Black (2007) state this species is a notorious bur- rows (Hobbs 1981; Peay and Dunn 2014). A decrease rower. Even among genetically uniform specimens, in water level may induce burrowing activity as behavioural plasticity in burrowing has been observed observed in P. clarkii by Correia and Ferreira (1995) (Linzmaier et al. 2018). and both increasing water temperature and increas- The present study observed that there were sig- ing light availability may act as early warning signals nificant differences in burrowing activity between for upcoming lower water levels (Boulton 2003). The females and males from the same species, with, for burrowing behaviour of P. clarkii has been related to example, less P. leptodactylus males burrowing com- drought avoidance (Hobbs 1981), and in the present pared to females when a shelter was present. Signifi- study P. clarkii was the only species that increased cant differences between sexes were also found for burrowing activity to both drought indicators. The P. acutus in the increased water temperature treat- response of P. clarkii was stronger to the water tem- ment and for P. leniusculus for the increased density perature increase than the light intensity increase with treatment. Especially during sensitive life history more specimens burrowing at higher water tempera- phases, use of shelters by crayfish is of great impor - tures. Pontastacus leptodactylus also increased bur- tance (Barbaresi et  al. 2004; Stoeckel et  al. 2011). rowing activity at increased light intensity but not For example, P. clarkii maternal females showed a with higher water temperatures which is in line with much stronger shelter competition and use than con- the observation by Valido et al. (2021). Interestingly, specific males or non-maternal females (Figler et  al. both drought triggers caused a total lack of response 2001; Haubrock et  al. 2019) and such shelter-related in F. limosus. This species generally occurs in all aggression seems to be quite common in decapods types of water bodies but prefers warmer, slow-flow - (Figler et  al. 1998). In addition, Haubrock et  al. ing and standing waters and is very tolerant to a vari- (2019) observed no differences between males and ety of environmental stressors and this high tolerance Vol.: (0123456789) 1 3 Aquat Ecol towards eutrophic conditions and water temperature managing crayfish populations and the problems they may explain the observed lack of response (Todorov cause. Like in many countries in Europe (e.g. Kouba et  al. 2020). Crayfish are in general night-active and et  al. 2014; Souty-Grosset et  al. 2016), the Nether- search more actively for shelter (Flint 1975, 1977) lands has to deal with several invasive crayfish spe- and occupy more shelters during day compared to cies (Lemmers et al. 2021; van Kuijk et al. 2021). The the night (Ranta and Lindström 2010; Thomas et  al. presence of these burrowing animals may increase 2016). Furthermore, increased artificial light during the risk of bank erosion (Harvey et al. 2019) resulting the night increased the time P. leniusculus spent in in concerns of dike collapses in peatland areas in the the shelter (Thomas et  al. 2016). Nevertheless, this Netherlands (Lemmers et al. 2021). High burrow den- study clearly indicate that the responses to drought sity by P. leniusculus had led to considerable damage triggers are species-specific. of river banks in the UK (Guan 1994) and burrow- The density treatment in this study could only be ing activity by P. clarkii in rice field dikes in Portugal applied to a limited number of species and gave inter- resulted in leakages and finally the collapse of these esting results. The response to this treatment seems delimiting banks (Fonseca et al. 1997; Holdich 1999). also species-specific with A. astacus and P. leniuscu- The most widespread invasive crayfish species in the lus showing less burrowing, P. leptodactylus having Netherlands are F. limosus and P. clarkii (van Kuijk no change in behaviour and F. virilis showing a larger et al. 2021). The present study showed that F. limosus proportion of specimens trying to escape. Studies greatly lowers burrowing activity when natural shel- have indicated that the number of burrows is uncor- ters are present. The Netherlands has an extensive and related with crayfish density (Guan 1994; Ilhéu et al. complex network of ditches and canals to discharge 2003; Haubrock et  al. 2019) and this seems to con- excess water (Verdonschot et  al. 2011). The sedi- tradict the results from this study except for P. lep- ment in those ditches and canals frequently consists todactylus. Unlike in field conditions where multiple of fine material and thus ideal for crayfish to burrow opportunities are present, there was only one place (Correia and Ferreira 1995; Barbaresi et  al. 2004). where the animals could dig a burrow in the present Intense management of these systems through fre- study. The lower burrowing activity of A. astacus and quent dredging and yearly thoroughly cleaning of the P. leniusculus could possibly be due to specimens vegetation in the water ways has resulted in a homo- interacting more with the other specimen present in geneous underwater environment. The lack of shelters the experimental arena than seeking shelter. Support in those environments is probably one of the most for this hypothesis comes from observations that dif- important triggers for F. limosus to burrow. Chang- ferences in levels of aggression determine access to ing the way of managing water courses and creating a limited shelter together with fighting constituting a more heterogeneous environment with more variabil- high proportion of total interactions in equally sized ity in natural shelters might help to refrain F. limosus pairs (Vorburger and Ribi 1999). An alternative from burrowing. explanation for the unoccupied shelters could be that The lack of shelters does not seem to be an the dominant crayfish prevented the subordinate one important trigger to burrow for the other wide- from using it. This was also observed by Gherardi and spread species P. clarkii in the Netherlands as dem- Daniels (2004) in an interspecies shelter occupancy onstrated in the control treatment of the present experiment where the dominant P. clarkii did not use experiment. Although the species did not burrow the shelter after evicting subordinate P. acutus acutus in ephemeral waters in Portugal, it did make use of from it. Unfortunately, no video recordings have been boulders and complex microhabitats in the wild to made in the present study to verify this. shelter (Aquiloni et  al. 2005). It might be valuable to investigate if adding complex habitats in other- Implications wise homogeneous environments may lower bur- rowing intensity of this species. In the present The results of the present experiments indicate study, P. clarkii clearly responded to the increased that the tested species showed a different burrow - water temperature which is in line with studies indi- ing response to the triggers they were exposed to. cating that crayfish demonstrated greater burrowing These species-specific responses are very relevant for activity with higher water temperatures (Flint 1977; Vol:. (1234567890) 1 3 Aquat Ecol Acknowledgements Many thanks to Rene van Wijgaarden Guan and Wiles 1997; Bubb et  al. 2002; Stanton and Jelle Touwen for their help with catching crayfish (P. leni- 2004). Although Ilhéu et  al. (2003) found no rela- usculus). We are grateful to two anonymous reviewers for their tionship between total burrow density and P. clarkii valuable comments. population size, the number of active burrows has Authors contribution EP: conceptualization, methodology, been positively correlated with the density of P. verification, formal analysis, visualization, supervision, writ- clarkii (Arce and Diéguez-Uribeondo 2015). Inter- ing—original draft. RV: investigation, verification, formal anal- estingly, P. clarkii seems to be an inefficient user ysis, visualization, writing—original draft. JE: investigation, of its burrows as Barbaresi et  al. (2004) found that methodology, writing—review and editing. ML: investigation, writing—review and editing. RH: investigation, writing— individuals stayed on average 6  h in a burrow and review and editing. IR: conceptualization, methodology, veri- once abandoned, they started excavating a new bur- fication, resources, supervision, writing—review and editing. row instead of reoccupying the old one in areas with dense P. clarkii populations. The inefficient use Data availability The data underlying this study are included of burrows in combination with warmer summers in the published article and can be found in Online Resource 2. due to climate change may lead to large amounts Declarations of removed bank sediments and possibly to col- lapses of dikes. For water managers, more insight is Conflict of interest All authors declare to have no competing needed in how to prevent such massive burrowing. interests. More knowledge on how to reduce burrowing activ- Open Access This article is licensed under a Creative Com- ity as well as more knowledge of factors governing mons Attribution 4.0 International License, which permits P. clarkii population dynamics are essential for a use, sharing, adaptation, distribution and reproduction in any proper managing these invaders. medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Crea- tive Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated Conclusion otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds In conclusion, the present experiment shows that bur- the permitted use, you will need to obtain permission directly rowing behaviour among freshwater crayfish is spe- from the copyright holder. To view a copy of this licence, visit cies-specific and for some species sex specific. This http:// creat iveco mmons. org/ licen ses/ by/4. 0/. study also shed light on how crayfish will alter their burrowing behaviour in response to climate change. Droughts are likely to increase in certain areas in the world, and our results show that early warning signals References of drought increase burrowing behaviour for certain Albertson LK, Daniels MD (2018) Crayfish ecosystem engi- species. The response to burrowing triggers is spe- neering effects on riverbed disturbance and topography cies-specific with lack of shelter as a strong driver to are mediated by size and behavior. Freshw Sci 37:836– burrow for A. astacus, F. limosus and F. virilis, while 844. https:// doi. org/ 10. 1086/ 700884 increased light intensity triggers burrowing behaviour Aquiloni L, Ilhéu M, Gherardi F (2005) Habitat use and disper- sal of the invasive crayfish Procambarus clarkii in ephem- in P. leptodactylus, P. acutus and P. clarkii and low- eral water bodies of Portugal. Mar Freshw Behav Physiol ered activity of F. limosus. Increased water tempera- 38:225–236. https:// doi. org/ 10. 1080/ 10236 24050 03101 95 ture was the most important trigger for P. clarkii to Arce JA, Diéguez-Uribeondo J (2015) Structural damage burrow. The presence of a conspecific reduced bur - caused by the invasive crayfish Procambarus clarkii (Girard, 1852) in rice fields of the Iberian Peninsula: a rowing activity in A. astacus and P. leniusculus and study case. Fund Appl Limnol 186:259–269. https:// doi. triggered F. virilis to escape. Testing in a field situa- org/ 10. 1127/ fal/ 2015/ 0715 tion whether more complex habitats indeed result in Barbaresi S, Gherardi F (2006) Experimental evidence for lower burrowing activity together with more knowl- homing in the red swamp crayfish, Procambarus clarkii. Bull Fr Pêche Piscic 380–381:1145–1154. https:// doi. org/ edge on the causes of the species-specific responses 10. 1051/ kmae: 20060 17 and population dynamics may help managing popula- tions of these invasive species. Vol.: (0123456789) 1 3 Aquat Ecol Flint RW (1977) Seasonal activity, migration and distribution Barbaresi S, Tricarico E, Gherardi F (2004) Factors inducing of the crayfish, Pacifastacus Ieniusculus, in Lake Tahoe. the intense burrowing activity of the red-swamp cray- Am Midl Nat 97:280–292. https:// doi. org/ 10. 2307/ 24250 fish, Procambarus clarkii, an invasive species. Natur- wissenschaften 91:342–345. https:// doi. org/ 10. 1007/ Florey CL, Moore PA (2019) Analysis and description of bur- s00114- 004- 0533-9 row structure in four species of freshwater crayfishes Berrill M, Chenoweth B (1982) The burrowing ability of non- (Decapoda: Astacoidea: Cambaridae) using photogram- burrowing crayfish. Am Midl Nat 108:199–201. https:// metry to recreate casts as 3D models. J Crustac Biol doi. org/ 10. 2307/ 24253 10 39:711–719. https:// doi. org/ 10. 1093/ jcbiol/ ruz075 Boulton AJ (2003) Parallels and contrasts in the effects of Fonseca JC, Marques JC, Madeira VMC (1997) Oxygen uptake drought on stream macroinvertebrate assemblages. Freshw inhibition in Procambarus clarkii, red swamp crayfish, Biol 48:1173–1185. https:// doi. org/ 10. 1046/j. 1365- 2427. by biogradable surfactants: an ecotechnological approach 2003. 01084.x for population control in rice fields. Freshw Crayfish Bubb DH, Lucas MC, Thom TJ (2002) Winter movements 11:235–242 and activity of signal crayfish Pacifastacus leniusculus Gherardi F, Daniels WH (2003) Dominance hierarchies and in an upland river, determined by radio telemetry. Hyd- status recognition in the crayfish Procambarus acutus robiologia 483:111–119. https:// doi. org/ 10. 1023/A: 10213 acutus. Can J Zool 81:1269–1281. https:// doi. org/ 10. 63109 155 1139/ z03- 107 Burras L, Blakewood G, Richard T, Huner JV (1995) Labora- Groza MI, Pop-Vancia V, Mireşan V (2016) Diel activity and tory observations on burrowing in different soils by com- use of multiple artificially constructed shelters in Astacus mercially important procambarid crayfish. Freshw Cray - leptodactylus (Decapoda: Astacidae). Biologia 71:1369– fish 10:427–434 1379. https:// doi. org/ 10. 1515/ biolog- 2016- 0167 Correia AM, Anastácio PM (2008) Shifts in aquatic macroin- Guan RZ (1994) Burrowing behaviour of signal crayfish, Paci- vertebrate biodiversity associated with the presence and fastacus leniusculus (Dana), in the river Great Ouse, Eng- size of an alien crayfish. Ecol Res 23:729–734. https:// doi. land. Freshwater Forum 4:144–168 org/ 10. 1007/ s11284- 007- 0433-5 Guan RZ, Wiles P (1997) The home range of signal crayfish in Correia AM, Ferreira O (1995) Burrowing behavior of the a British lowland river. Freshwater Forum 8:45–54 introduced red swamp crayfish Procambarus clarkii Guo W, Hossain MS, Kubec J et al (2020) Psychoactive com- (Decapoda: Cambaridae) in Portugal. J Crustacean Biol pounds at environmental concentration alter burrowing 15:248–257. https:// doi. org/ 10. 2307/ 15489 53 behavior in the freshwater crayfish. Sci Total Environ Crandall KA, De Grave S (2017) An updated classification of 711:135138. https:// doi. org/ 10. 1016/j. scito tenv. 2019. the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. J Crustacean Biol Harvey GL, Henshaw AJ, Brasington J, England J (2019) Bur- 37:615–653. https:// doi. org/ 10. 1093/ jcbiol/ rux070 rowing invasive species: an unquantified erosion risk at Emery-Butcher HE, Beatty SJ, Robson BJ (2023) Seasonal and the aquatic-terrestrial interface. Rev Geophys 57:1018– perennial water populations of an endemic crayfish differ 1036. https:// doi. org/ 10. 1029/ 2018R G0006 35 in behavioural responses to drying but not metabolism. Hasiotis ST (1995) Notes on the burrow morphologies and Ecohydrology. https:// doi. org/ 10. 1002/ eco. 2566 Faller M, Harvey GL, Henshaw AJ et al (2016) River bank bur- nesting behaviors of adults and juveniles of Procambarus rowing by invasive crayfish: spatial distribution, biophysi- clarkii and Procambarus acutus acutus (Decapoda: Cam- cal controls and biogeomorphic significance. Sci Total baridae). Freshw Crayfish 8:623–634. https:// doi. org/ 10. Environ 569–570:1190–1200. https:// doi. org/ 10. 1016/j. 5869/ fc. 1995. v8. 623 scito tenv. 2016. 06. 194 Haubrock PJ, Inghilesi AF, Mazza G et  al (2019) Burrow- Fernández-De-Miguel F, Aréchiga H (1992) Sensory inputs ing activity of Procambarus clarkii on levees: analys- mediating two opposite behavioural responses to light in ing behaviour and burrow structure. Wetl Ecol Manag the crayfish Procambarus clarkii. J Exp B 164:153–169. 27:497–511. https:// doi. org/ 10. 1007/ s11273- 019- 09674-3 https:// doi. org/ 10. 1242/ jeb. 164.1. 153 Hobbs HH (1981) The crayfishes of Georgia. Smithson Contrib Field A (2013) Discovering statistics using IBM SPSS statis- Zool. https:// doi. org/ 10. 5479/ si. 00810 282. 318 tics, 4th edn. SAGE Publications, London Holdich DM (1999) The negative effects of established crayfish Figler MH, Peeke HVS, Chang ES (1998) Shelter-related introductions. In: Gherardi F (ed) Crayfish in Europe as aggression between adult male conspecific intruders and Alien Species, 1st edn. Routledge, Milton Park, pp 31–47. resident maternal American lobsters (Homarus ameri-https:// doi. org/ 10. 1201/ 97813 15140 469 canus) with eggs at different stages of embryogenesis. Holdich D, Black J (2007) The spiny-cheek crayfish, Mar Freshw Behav Physiol 31:151–166. https:// doi. org/ Orconectes limosus (Rafinesque, 1817) [Crustacea: 10. 1080/ 10236 24980 93870 70 Decapoda: Cambaridae], digs into the UK. Aquat Inva- Figler MH, Blank GS, Peeke HVS (2001) Maternal territorial- sions 2:1–15. https:// doi. org/ 10. 3391/ ai. 2007.2. 1.1 ity as an offspring defense strategy in red swamp crayfish Ilhéu M, Acquistapace P, Benvenuto C, Gherardi F (2003) (Procambarus clarkii, Girard). Aggress Behav 27:391– Shelter use of the red-swamp crayfish (Procambarus 403. https:// doi. org/ 10. 1002/ ab. 1024 clarkii) in dry-season stream pools. Arch Hydrobiol Flint RW (1975) The natural history, ecology and production 157:535–546. https:// doi. org/ 10. 1127/ 0003- 9136/ 2003/ of the crayfish, Pacifastacus leniusculus, in a subalpine 0157- 0535 lacustrine environment. University of California, Davis Vol:. (1234567890) 1 3 Aquat Ecol Netherlands. Aquat Invasions 12:397–404. https:// doi. org/ Kaestner A (1991) Lehrbuch der Speziellen Zoologie. Band I. 10. 3391/ ai. 2017. 12.3. 12 Wirbellose. 2. Teil. Crustacea. Fisher Romaire RP, Lutz CG (1989) Population dynamics of Pro- Kouba A, Petrusek A, Kozak P (2014) Continental-wide dis- cambarus clarkii (Girard) and Procambarus acutus acu- tribution of crayfish species in Europe: update and maps. tus (Girard) (Decapoda: Cambaridae) in commercial Knowl Manag Aquat Ec 413:05. https:// doi. org/ 10. 1051/ ponds. Aquaculture 81:253–274. https:// doi. org/ 10. 1016/ kmae/ 201400 0044- 8486(89) 90151-8 Kouba A, Tíkal J, Císař P et  al (2016) The significance of Sanders H, Rice SP, Wood PJ (2021) Signal crayfish burrow - droughts for hyporheic dwellers: evidence from freshwater ing, bank retreat and sediment supply to rivers: a biophys- crayfish. Sci Rep 6:26569. https:// doi. org/ 10. 1038/ srep2 ical sediment budget. Earth Surf Process Landf 46:837– 852. https:// doi. org/ 10. 1002/ esp. 5070 Lemmers P, Collas F, Gylstra R et  al (2021) Risks and man- Souty-Grosset C, Reynolds J, Gherardi F et al (2014) Burrow- agement of alien freshwater crayfish species in the Rhine- ing activity of the invasive red swamp crayfish, Procamb- Meuse river district. Manag Biol Invasions 12:193–220. arus clarkii, in fishponds of la Brenne (France). Ethol https:// doi. org/ 10. 3391/ mbi. 2021. 12.1. 13 Ecol Evol 26:263–276. https:// doi. org/ 10. 1080/ 03949 370. Linzmaier SM, Goebel LS, Ruland F, Jeschke JM (2018) 2014. 892538 Behavioral differences in an over-invasion scenario: Souty-Grosset C, Anastácio PM, Aquiloni L et  al (2016) The marbled vs. spiny-cheek crayfish. Ecosphere 9:e02385. red swamp crayfish Procambarus clarkii in Europe: https:// doi. org/ 10. 1002/ ecs2. 2385 impacts on aquatic ecosystems and human well-being. McClain WR (2013) Effects of simulated precipitation Limnologica 58:78–93. https:// doi. org/ 10. 1016/j. limno. extremes on crayfish (Procambarus clarkii Girard) ovi- 2016. 03. 003 position in artificial burrows. Aquac Res 44:612–617. Stanton JA (2004) Burrowing behaviour and movements of the https:// doi. org/ 10. 1111/j. 1365- 2109. 2011. 03066.x signal crayfish Pacifastacus leniusculus (Dana). Thesis, Mojžišová M, Mrugała A, Kozubíková-Balcarová E et  al University of Leicester (2020) Crayfish plague in Czechia: outbreaks from Statzner B, Fièvet E, Champagne J-Y et  al (2000) Crayfish as novel sources and testing for chronic infections. J Inver- geomorphic agents and ecosystem engineers: biological tebr Pathol 173:107390. https:// doi. org/ 10. 1016/j. jip. behavior affects sand and gravel erosion in experimental 2020. 107390 streams. Limnol Oceanogr 45:1030–1040. https:// doi. org/ Mojžišová M, Svobodová J, Kozubíková-Balcarová E et  al 10. 4319/ lo. 2000. 45.5. 1030 (2022) Long-term changes in the prevalence of the Statzner B, Peltret O, Tomanova S (2003) Crayfish as geomor - crayfish plague pathogen and its genotyping in inva- phic agents and ecosystem engineers: effect of a biomass sive crayfish species in Czechia. NeoBiota 74:105–127. gradient on baseflow and flood-induced transport of gravel https:// doi. org/ 10. 3897/ NEOBI OTA. 74. 79087 and sand in experimental streams. Freshw Biol 48:147– Nystrom P, Strand JA (1996) Grazing by a native and an 163. https:// doi. org/ 10. 1046/j. 1365- 2427. 2003. 00984.x exotic crayfish on aquatic macrophytes. Freshw Biol Stoeckel JA, Helms BS, Cash E (2011) Evaluation of a crayfish 36:673–682. https:// doi. org/ 10. 1046/j. 1365- 2427. 1996. burrowing chamber design with simulated groundwater d01- 508.x flow. J Crustacean Biol 31:50–58. https:// doi. org/ 10. 1651/ Nystrom P, Bronmark C, Graneli W (1999) Influence of an exotic and a native crayfish species on a littoral benthic 09- 3271.1 community. Oikos 85:545. https:// doi. org/ 10. 2307/ 35467 Suzuki T, Arikawa K, Eguchi E (1985) The effects of light and 04 temperature on rhodopsin-porphyropsin visual system of Payette AL, McGaw IJ (2003) Thermoregulatory behavior of the crayfish, Procambarus clarkii. Zoolog Sci 2:455–461 the crayfish Procambarus clarki in a burrow environment. Thomas JR, James J, Newman RC et  al (2016) The impact of Comp Biochem Phys A 136:539–556. https:// doi. org/ 10. streetlights on an aquatic invasive species: artificial light 1016/ S1095- 6433(03) 00203-4 at night alters signal crayfish behaviour. Appl Anim Behav Peay S, Dunn AM (2014) The behavioural response of the Sci 176:143–149. https:// doi. org/ 10. 1016/j. appla nim. invasive signal crayfish Pacifastacus leniusculus to 2015. 11. 020 experimental dewatering of burrows and its implications Tilmans M, Mrugała A, Svoboda J et  al (2014) Survey of the for eradication treatment and management of ponds with crayfish plague pathogen presence in the Netherlands crayfish. Ethol Ecol Evol 26:277–298. https:// doi. org/ 10. reveals a new Aphanomyces astaci carrier. J Invertebr 1080/ 03949 370. 2014. 903379 Pathol 120:74–79. https:// doi. org/ 10. 1016/j. jip. 2014. 06. Ranta E, Lindström K (2010) Power to hold sheltering burrows 002 by juveniles of the signal crayfish, Pasifastacus leniuscu- Todorov M, Trichkova T, Hubenov Z, Jurajda P (2020) Faxo- lus. Ethology 92:217–226. https:// doi. org/ 10. 1111/j. 1439- nius limosus (Rafinesque, 1817) (Decapoda: Cambaridae), 0310. 1992. tb009 61.x a new invasive alien species of European Union concern Reynolds J, Souty-Grosset C, Richardson A (2012) Crayfish in Bulgaria. Acta Zool Bulgar 72:113–121 as prime players in ecosystems: life-history strategies. In: Valido CAR, Johnson MF, Dugdale SJ et  al (2021) Thermal Reynolds J, Souty-Grosset C (eds) Management of fresh- sensitivity of feeding and burrowing activity of an inva- water biodiversity: crayfish as bioindicators. Cambridge sive crayfish in UK waters. Ecohydrology 14:e2258. University Press, Cambridge, pp 59–82https:// doi. org/ 10. 1002/ eco. 2258 Roessink I, Gylstra R, Heuts P et al (2017) Impact of invasive van Kuijk T, Biesmeijer JC, van der Hoorn BB, Verdonschot crayfish on water quality and aquatic macrophytes in the PFM (2021) Functional traits explain crayfish invasive Vol.: (0123456789) 1 3 Aquat Ecol success in the Netherlands. Sci Rep 11:2772. https:// doi. Weber S, Traunspurger W (2017) Invasive red swamp crayfish org/ 10. 1038/ s41598- 021- 82302-4 (Procambarus clarkii) and native noble crayfish (Astacus Verdonschot RCM, Keizer-vlek HE, Verdonschot PFM (2011) astacus) similarly reduce oligochaetes, epipelic algae, Biodiversity value of agricultural drainage ditches: a and meiofauna biomass: a microcosm study. Freshw Sci comparative analysis of the aquatic invertebrate fauna 36:103–112. https:// doi. org/ 10. 1086/ 690556 of ditches and small lakes. Aquat Conserv 21:715–727. https:// doi. org/ 10. 1002/ aqc. 1220 Publisher’s Note Springer Nature remains neutral with regard to Vorburger C, Ribi G (1999) Aggression and competition for jurisdictional claims in published maps and institutional affiliations. shelter between a native and an introduced crayfish in Europe. Freshw Biol 42:111–119. https:// doi. org/ 10. 1046/j. 1365- 2427. 1999. 00465.x Vol:. (1234567890) 1 3 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Aquatic Ecology Springer Journals

Triggers affecting crayfish burrowing behaviour

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Aquat Ecol https://doi.org/10.1007/s10452-023-10057-3 Edwin T. H. M. Peeters  · Robin de Vries · Jesper Elzinga · Mercédesz Ludányi · Robbert van Himbeeck · Ivo Roessink Received: 8 May 2023 / Accepted: 29 August 2023 © The Author(s) 2023 Abstract Surface water inhabiting crayfish are burrowing was investigated under standardized labo- well-known for the impact on their surroundings. ratory conditions to reveal differences among species This impact has been related to loss of biodiversity and their sex. All studied species occur in the Neth- and deteriorating water quality for invasive crayfish. erlands and were the native Astacus astacus (Lin- Crayfish dig burrows for various reasons like lack of naeus, 1758), the Eurasian Pontastacus leptodactylus natural shelters, avoiding an upcoming drought, or (Eschscholtz, 1823) and the invasive North American high crayfish density and this may lead to increased Faxonius virilis (Hagen, 1870), F. limosus (Rafin- sediment transport and accelerated bank instability. esque 1817), Pacifastacus leniusculus (Dana, 1852), All crayfish are considered to have burrowing capa- Procambarus acutus (Girard 1852), and P. clarkii bility, but not all species have been observed burrow- (Girard, 1852). As burrowing triggers were evalu- ing. Studies comparing this behaviour among differ - ated presence of shelter, increased light intensity, ent species in standardized ways are scarce. Crayfish increased water temperature, and increased crayfish density. Results showed species-specific and some- times sex-specific differences in burrowing behaviour Handling editor: Télesphore Sime-Ngando. among crayfish. The response to burrowing triggers Supplementary Information The online version was also species-specific and no two species reacted contains supplementary material available at https:// doi. identical to all triggers. Absence of shelter was a org/ 10. 1007/ s10452- 023- 10057-3. E. T. H. M. Peeters (*) · R. de Vries · J. Elzinga · Present Address: M. Ludányi · R. van Himbeeck  M. Ludányi  Chairgroup Aquatic Ecology and Water Quality BioAqua Pro Ltd., Debrecen, Hungary Management, Wageningen University, Wageningen, The Netherlands Present Address: e-mail: edwin.peeters@wur.nl R. van Himbeeck  Laboratory of Nematology, Wageningen University, Present Address: Wageningen, The Netherlands R. de Vries  Wageningen, The Netherlands I. Roessink  Environmental Risk Assessment Group, Wageningen Present Address: Environmental Research, Wageningen, The Netherlands J. Elzinga  Environmental Engineering Department, Van Oordt Dredging and Marine Contractors, Rotterdam, The Netherlands Vol.: (0123456789) 1 3 Aquat Ecol strong driver to burrow for A. astacus, F. limosus and 2016; Roessink et  al. 2017). Furthermore, the bur- F. virilis, while increased light intensity triggered rows they dig may lead to increased sediment trans- burrowing behaviour in P. leptodactylus, P. acutus port in streams (Sanders et  al. 2021) and may cause and P. clarkii and lowered activity of F. limosus. Bur- or accelerate river bank instability and erosion (Arce rowing behaviour of P. clarkii was mostly influenced and Diéguez-Uribeondo 2015; Faller et  al. 2016; by increased water temperature. Significant differ - Harvey et  al. 2019), collapse of delimiting banks ences between females and males were observed for in rice fields (Arce and Diéguez-Uribeondo 2015), P. leptodactylus, P. leniusculus and P. acutus in the and increase the risk of compromised riverbanks in shelter, increased density and increased water tem- peatland areas (Lemmers et  al. 2021). Although all perature treatment, respectively. Understanding the freshwater crayfish species have the ability to burrow triggers that invoke burrowing may help managing (Hobbs 1981; Crandall and De Grave 2017; Florey populations of these invasive species. and Moore 2019), there is also a number of crayfish species that live in permanent water which burrow- Keywords Density · Invasive species · Light ing may be limited (Berrill and Chenoweth 1982). intensity · Shelter · Water temperature These observations have been made under different field conditions and studies that compare this burrow - ing capacity among species under similar conditions Introduction are very scarce but see e.g. Burras et  al. (1995) and Kouba et al. (2016). Crayfish that inhabit open waters (tertiary and sec- It is generally accepted that burrows function as a ondary burrowers) are well-known for their impact means to withstand environmental extremes (e.g. high on the surrounding biotic and abiotic environment temperatures) and as a protection against predators, (Hobbs 1981). Due to this profound effect on their especially during sensitive life history phases (Barba- environment they are regarded as ecosystem engi- resi et al. 2004; Stoeckel et al. 2011). But what triggers neers (Statzner et  al. 2003; Albertson and Daniels burrowing behaviour in the different crayfish species? 2018). Through their feeding and foraging behav- Although burrowing might be a direct result of envi- iour, crayfish can have a great negative impact on ronmental stress (Correia and Ferreira 1995), triggers benthic macroinvertebrate communities (Correia and for this behaviour seem rather unpredictable (Barbaresi Anastácio 2008; Souty-Grosset et  al. 2016). This and Gherardi 2006). An important reason for crayfish may result in less biodiverse communities in places to excavate is seeking shelter as burrowing appeared to where they occur compared to places where they are be inversely related to the availability of natural shel- absent. The impact of invasive crayfish on the native ters present (Flint 1975; Berrill and Chenoweth 1982; macroinvertebrate community can be either compa- Ilhéu et  al. 2003). Burrowing activities can be up to rable to (Weber and Traunspurger 2017) or greater five times higher when there is a lack of protection but (Nystrom et al. 1999) than the impact native crayfish depends of the bottom structure (Flint 1975). Crayfish have. Since almost all invasive species are carriers leave shelters for feeding during the night because risk of the crayfish plague, their presence obviously limit of predation is lower, and this risk increases parallel the distribution of native species in Europe (Tilmans to increasing light intensities (Flint 1975; Ranta and et  al. 2014; Souty-Grosset et  al. 2016; Mojžišová Lindström 2010). The observed withdrawal of crayfish et  al. 2020, 2022). Crayfish species may also nega- towards their burrows when light intensities increased tively affect emergent, floating or submerged plants (Suzuki et al. 1985; Fernández-De-Miguel and Aréch- by grazing (Nystrom and Strand 1996) and, especially iga 1992) supports the notion that burrowing and light the loss of submerged plants may lead to increased intensity might be correlated. Increasing light intensity turbidity of the water (Roessink et  al. 2017). The can also act as an early warning signal for an upcoming relatively substantial individual body size in combi- drought that can have a detrimental effect on crayfish nation with their behaviour (walking, fighting, for - populations (McClain 2013; Kouba et  al. 2016). Sur- aging) and eventually high population densities may vival of crayfish outside of water is species dependent lead to physical disturbance of the sediment that (Reynolds et  al. 2012), and a link has been observed negatively affects water quality (Souty-Grosset et  al. between drought and burrowing activities (Correia and Vol:. (1234567890) 1 3 Aquat Ecol Ferreira 1995; Barbaresi et al. 2004). Increase in water bath (see pictures of Online Resource 1) to ensure a temperature is another signal that can be associated stable and comparable water temperature (18–20 °C). with dry periods (Boulton 2003) and higher water tem- Each crate had an additional PVC wall installed peratures stimulate the activity and metabolism of cray- to mimic a bank and to create a visual wall for the fish (Flint 1975). Furthermore, biological factors like crayfish. Two openings in this wall provided access crayfish density may affect burrow use with a higher to a PVC pipe (Ø 5.8  cm) with one filled with 25 occupancy rate of burrows at higher P. clarkii densities blue foam blocks of 3–4  cm to provide burrowing (Ranta and Lindström 2010). Although no relationship opportunities, and the other pipe open to provide a seems to exist between burrow density and P. clarkii shelter or closed off, depending on the treatment. population size (Ilhéu et al. 2003), the number of active Copper-free tap water was used to fill the crates burrows has been positively correlated with the popu- until ten centimetres below the top (48  L), minimiz- lation size (Arce and Diéguez-Uribeondo 2015). Bur- ing escapes. Aeration via a tube with an air stone rowing behaviour has also been linked to the reproduc- was provided in each crate to maintain stable dis- tive cycle (Romaire and Lutz 1989; Holdich and Black solved oxygen levels, while a shade cloth above the 2007) with earlier burrowing activity in the season creates prevented stress caused by too high artificial by female P. leniusculus (Stanton 2004), larger and light intensity as shown in the pictures of Online deeper burrows by female P. clarkii (Guo et  al. 2020) Resource 1. Light intensity under the shade cloth but −2 −1 and, especially females with eggs retreating in burrows above the crates averaged around 85  µmol  m  s −2 −1 (Hasiotis 1995).(range 74–100 µmol  m  s ). A day-night regime of Currently, there are several invasive crayfish spe- 10–14 h was applied. cies with well-established populations in the Neth- Each treatment (Table  1) was tested for three suc- erlands while only one species is native (Lemmers cessive days. Twelve crates per run were available and et al. 2021). This offers the opportunity to study bur - in each run six males and six females were deployed. rowing behaviour in a standardized way among dif- Depending on the availability of animals and time, in ferent crayfish species. The prime aim of the present principle two runs were performed per species and study was to investigate crayfish burrowing behav - treatment, giving twelve observations per sex for one iour and reveal possible differences among seven treatment. All runs for a species were usually per- crayfish species and their sex. The second aim was formed within a period of two months. To minimize to identify which triggers invoke this behaviour. In human impact on crayfish behaviour, the room with a laboratory experimental set-up, four possible trig- the water bath was only accessed by the observers gers, namely the presence of shelter, increased light to daily check the well-being of all individuals dur- intensity, increased water temperature, and increased ing a run. After each run, all materials were cleaned crayfish density were evaluated for burrowing behav - with fresh water and the crates were refilled with iour in the native species Astacus astacus (Linnaeus, new water to remove any odour from previous cray- 1758), the Eurasian species Pontastacus leptodactylus fish. In case a crayfish removed at least three blocks (Eschscholtz, 1823) non-native to the Netherlands, (out of 25) from the pipe, this was regarded as bur- and the invasive North American species Faxonius rowing behaviour. In a number of cases, crayfish tried virilis (Hagen, 1870), Faxonius limosus (Rafinesque, to escape the crate and when this occurred this was 1817), Pacifastacus leniusculus (Dana, 1852), Pro- recorded as an escape response. The first response cambarus acutus (Girard, 1852), and Procambarus (digging or escaping) determined the result for that clarkii (Girard, 1852). crayfish for that treatment. Treatments Materials and methods Five different treatments were tested (Table  1). In the General set-up burrowing experiment control treatment, the one PVC pipe in the crates was covered with a PVC plate while the other pipe was Twelve plastic crates of 60 × 40 × 30 filled with the blue foam blocks (size approximately (length × width × height) cm were placed in a water 1.5 × 1.5 × 1.5  cm). Crayfish were allowed to burrow Vol.: (0123456789) 1 3 Aquat Ecol Table 1 Overview of tested treatments. All treatments had a standard water temperature (18–20 °C) and a standard light intensity −2 −1 (85 μmol  m  s ) and one crayfish per crate unless stated otherwise Treatment Description Schematic representation Control One pipe filled with blue foam and the other pipe blocked by a PVC plate Shelter As the Control treatment, but with one additional empty pipe representing a place to shelter Increased light intensity As the Control treatment but light intensity above the crate was −2 −1 increased in two days to an average of 200–280 µmol  m  s after 1 run-in day Increased water temperature As the control treatment but temperature of the water in the crate was increased in two day with 3 °C per day (6 °C in total) after 1 run-in day Increased crayfish density As the control treatment but a second crayfish was introduced in the tank. At the start of the experiment, the crayfish were sepa- rated from each other for 10 min with a perspex T-structure Drawing crayfish by Pearson Scott Foresman for nearly three days (66 h including, two nights). In intensity. After this pre-treatment night, the treat- the shelter treatment, the pipe with foam was avail- ment started by increasing the light intensity above −2 −1 able and from the other pipe the cover was removed the crates during daytime to 200–80 µmol  m  s by to provide a shelter possibility. The increased light adapting the emitted intensity of the artificial lamps intensity treatment started with one day (one night) to the required level. Crayfish were again offered to of acclimatization to the conditions that correspond burrow for three days (two nights). The increased to the control treatment with only the pipe filled with water temperature treatment also started with one day foam available. All crayfish that showed a response (one night) of acclimatization to the control treatment within this one day were removed from the treatment conditions with again only the pipe filled with foam because the response was not triggered by higher light available. Crayfish that showed a response within this Vol:. (1234567890) 1 3 Aquat Ecol one day were removed from the treatment because the sex and length of carapace were determined. Due to response was not triggered by higher water tempera- logistical issues, not all treatments were tested for ture. After the pre-treatment, water temperature was all species by sex combinations. Control and shelter gradually increased with 3 °C per day until it reached treatment were performed for all species but both 26 °C by increasing the temperature of the water bath. sexes of F. virilis could not be tested for increased For the density treatment, crayfish were individually light intensity and increased water temperature and placed in buckets 24  h before the start of the test to both sexes of F. limosus, P. acutus and P. clarkii were ensure that they were free from odours of other cray- not tested for density effects. Each crayfish specimen fish in their housing tank. Thereafter, they were trans- was in principle used in all tests and were given at ferred into the crates under similar conditions as the least seven days between two trials to recover. control treatment. In each container two individuals from the same sex and species were introduced and a divider separated the individuals for the first ten min- Data analysis utes to let them get used to each other’s smell, with- out seeing each other. The divider was removed and Both the water temperature and light intensity treat- both crayfish were free to burrow. ment had an one day run-in period using the standard conditions from the control experiment. Specimens Crayfish that showed a response during this first day and night were removed from the treatment. As a consequence, Seven crayfish species were tested over the years a lower number of replicates for that treatment was (Table  2). Most invasive crayfish were wild-caught available for statistical testing and for some species by either local fisherman or by the staff. Faxonius the number of observations became lower than a-pri- limosus and P. clarkii originated from Hardinxveld- ori anticipated. Density treatment was always per- Giessendam (the Netherlands), F. virilis from the formed at the end of the series of tests. This was done floodplains of the river Waal near Boven-Leeuwen to avoid damages that may arise when specimens (the Netherlands), and P. leniusculus from the Oude fight with each other, so we ensured that all other Leij in Tilburg (the Netherlands). Procambarus acu- tested treatments were performed with intact animals. tus originated from a culture (Harald Groβ, Edelkrebs The number of times that burrowing, escaping and und Fischzucht, DE) and P. leptodactylus frome a no responses occurred were determined per treat- commercial supplier (Koidreams, Valburg, NL) while ment and per species and sex. Fisher’s exact tests Astacus astacus came from an own culture. in SPSS (Field 2013) were applied to test whether Prior to the experiment, crayfish were housed the observed responses (burrowing, escaping or no separately to avoid fights and injuries. Three pellets response) of a single species (females and males of Trouvit (Skretting, a Nutreco company) were fed separately and taken together) in a specific treat- to each crayfish twice a week. Each individual got an ment significantly differed from the control treat- unique number written with Tipp-Ex on the carapace ment. Adjusted standardized residuals were evaluated for individual recognition during the experiment and to discover which observed response deviated from Table 2 Overview of the Species English name Origin Period of testing n seven species, their origin, period of testing (month Astacus astacus Noble crayfish Europe 06–2015 24 and year), and available Pontastacus leptodactylus Narrow-clawed crayfish Eurasia 05–2015 23 number of specimens (n) Pacifastacus leniusculus Signal crayfish North America 09–2016 till 50 for the experiment 01–2017 Faxonius limosus Spiny-cheek crayfish North America 04–2013 23 Faxonius virilis Virile crayfish North America 04–2016 24 Procambarus acutus White river crayfish North America 04–2013 21 Procambarus clarkii Red swamp crayfish North America 04–2013 22 Vol.: (0123456789) 1 3 Aquat Ecol Vol:. (1234567890) 1 3 Aquat Ecol Fig. 1 Relative distribution of responses for all treatments for ◂ shelter, increased light intensity, and increased the tested seven species separated by sex. No bar means not water temperature treatment, all specimen showed tested, except for male A. astacus, that responded already in no response and the difference with the control the acclimatization period of the increased light intensity and treatment was significant (Table  4) except for the increased water temperature treatment. F = females, M = males increased water temperature treatment due to the lower number of observations in this treatment. the expectation. A p value ≤ 0.05 indicated a signifi- These differences were mainly due to changes in the cant difference while a value between 0.05 and 0.10 behaviour of the females. was regarded as indicating a trend. Fisher’s exact test Faxonius virilis actively burrowed in the control was also used to statistically evaluate the differences treatment (Fig.  1) and offering shelter significantly between sexes per species in the different treatments (Table  4) reduced the number of burrowing speci- and to evaluate differences between species. mens. In the increased crayfish density treatment, significantly more specimens tried to escape the experimental setting. Results Approximately half of P. leniusculus specimens burrowed in the control treatment (Fig.  1) and the Figure 1 shows a summary of the obtained results and shelter and increased light intensity treatment did the raw data counts can be found in Online Resource not result in significant changes in behaviour. In the 2. increased water temperature and increased crayfish density treatments, one third of the males and none Sex-specific response behaviour of the females burrowed and the difference of the latter with the control treatment were significant In a number of cases, the response of females to a (Table 4). treatment differed significantly from males (Fig.  1, Around 40–50% of P. leptodactylus burrowed Table  3). Significantly (p ≤ 0.05) less P. leptodac- in the control treatment (Fig.  1) and in the shelter tylus males burrowed in the shelter treatment, less treatment only males burrowed significantly less P. acutus males in the increased water temperature (Table 4). In the increased light intensity treatment, treatment and more P. leniusculus males burrowed in significantly more specimens burrowed which was the increased crayfish density treatment. There was due to the males. No significant differences were a trend (0.05 < p ≤ 0.10) in more P. acutus females observed due to the increased water temperature or showing no response in the shelter treatment and increased crayfish density. less P. leniusculus females showing a response in the Roughly 10% of P. acutus specimens burrowed in increased water temperature treatment. the control treatment (Fig.  1) and this did not sig- nificantly (Table  4) change in the shelter treatment Species-specific response behaviour despite the trend in response between females and males. In the increased light intensity and increased Astacus astacus was an active burrower (95% of the water temperature treatment, more specimens specimen) in the control treatment (Fig.  1), and bur- showed a response but this was not significant. rowing activity was significantly (Table  4) lower in Less than 5% of the P. clarkii specimens bur- the shelter treatment. All males responded during the rowed in the control treatment (Fig. 1) and a similar acclimatization period for both the increased light pattern was observed for the shelter treatment which intensity and increased water temperature treatment. was not significantly (Table  4) different from the Increased light intensity resulted in a trend with fewer control treatment. Both increased light intensity and females burrowing compared to the control treatment. increased water temperature significantly reduced Increased water temperature did not lead to significant the number of specimens without a response in changes in females. Increased crayfish density signifi- favour of more burrowing or males trying to escape. cantly lowered burrowing activity in this species. A quarter of the specimens of F. limosus bur- rowed in the control treatment (Fig.  1). In the Vol.: (0123456789) 1 3 Aquat Ecol Table 3 Results of Fisher’s exact test (Chi-square, p value, degree of freedom, total observations) to evaluate the significance of sex per species Treatment Fisher’s Test A. astacus P. leptodactylus P. leniusculus F. limosus F. virilis P. acutus P. clarkii Control χ2 1.043 0.436 1.387 4.346 1.846 1.143 1.210 p 1.000 0.407 0.531 0.104 0.482 0.803 1.000 df 1 1 2 2 1 2 2 n 24 23 50 23 24 21 22 Shelter χ2 1.423 8.224 1.938 Constant 0.938 4.090 Constant p 0.796 0.006 0.580 1.000 0.095 df 2 1 2 2 2 n 21 24 26 24 24 15 14 Increased light availability χ2 N.D 2.250 1.869 Constant N.A 1.044 0.938 p 0.333 0.608 0.807 1.000 df 1 2 2 2 n 9 15 21 20 15 Increased water temperature χ2 N.D 1.400 4.550 Constant N.A 8.507 3.497 p 0.280 0.070 0.009 0.257 df 1 2 2 2 n 14 13 9 22 14 Increased crayfish density χ2 0.133 0.105 4.800 N.A 2.630 N.A N.A p 1.000 1.000 0.047 0.315 df 1 1 1 2 n 26 22 24 16 N.A.: not tested at all, N.D.: no data available because all specimens from one sex escaped during the acclimatization period, Con- stant: no variability in response due to the exact same response by females and males Significant (p ≤ 0.05) differences between females and males are in bold and italic and trends (0.05 < p ≤ 0.10) in bold only Differences in response behaviour among species virilis specimens showed this escape behaviour in the density experiment. Both Procambarus species were The species tested in the treatments showed signifi- triggered to burrow by increased light intensity and cantly different behaviour (Table  5). Astacus asta- especially increased water temperature. The increased cus and F. virilis burrowed significantly more in the water temperature treatment resulted in the highest control treatment while only a small fraction of F. response of P. clarkii to stimuli. Increased light inten- limosus and both Procambarus species burrowed. A sity also triggered male P. leptodactylus to dig. The similar pattern was observed in the shelter treatment. increased crayfish density treatment triggered F. viri- In the increased light and increased water temperature lis to escape, a response that was not observed for the treatment, P. leptodactylus burried more frequently other species. than the other tested species F. limosus, P. lenius- culus and both Procambarus species. Pacifastacus leniusculus burrowed less than P. leptodactylus, F. Discussion virilis and A. astacus while F. virilis more frequently escaped. In this laboratory study, crayfish were placed in an Roughly 50% of A. astacus and P. leptodactylus artificial environment with one pipe filled with pieces dug in all treatments (Fig. 1) which is in contrast with of foam to study their burrowing behaviour. Pipes of the lack of burrowing in a number of treatments for F. comparable diameter have been successfully used as limosus, P. acutus and P. clarkii. Procambarus acu- shelters in other experiments with tertiary crayfish tus and P. clarkii and male P. leniusculus more fre- (Gherardi and Daniels 2003; Payette and McGaw quently escaped than the other species. Half of the F. 2003; Stanton 2004; Barbaresi and Gherardi 2006) Vol:. (1234567890) 1 3 Aquat Ecol Table 4 Results of Fisher’s exact test (Chi-square, p value, degree of freedom, number of observations) to evaluate the significance of observed difference in behaviour between the treatment and control Species Shelter Increased light intensity Increased water tempera- Increased crayfish density ture χ2 p df n χ2 p df n χ2 p df n χ2 p df n A. astacus 7.887 0.009 2 45 11.435 < 0.001 1 50 F 5.972 0.021 2 21 4.500 0.098 1 18 2.976 0.217 2 24 8.000 0.007 1 24 M 2.403 0.158 1 24 N.D N.D 3.914 0.060 1 26 P. leptodactylus 0.260 0.552 1 47 5.420 0.024 1 32 0.149 0.481 1 37 0.237 0.428 1 45 F 1.623 0.200 1 24 0.268 0.554 1 15 0.220 0.485 1 22 0.686 0.340 1 24 M 1.168 0.275 1 23 6.491 0.017 1 17 0.170 0.593 1 15 0.029 0.608 1 21 P. leniusculus 2.213 0.379 2 76 1.740 0.401 2 65 4.877 0.071 2 63 9.058 0.007 2 74 F 3.184 0.216 2 39 0.907 0.797 2 33 8.018 0.013 2 33 13.282 < 0.001 2 38 M 1.616 0.594 2 37 2.932 0.268 2 32 1.607 0.590 2 30 0.864 0.814 2 36 F. limosus 8.562 0.004 2 47 7.586 0.014 2 44 3.216 0.188 2 32 N.A F 7.738 0.014 2 24 7.181 0.023 2 23 4.129 0.150 2 18 N.A M 1.140 0.478 1 23 1.339 0.524 1 21 0.294 0.786 1 14 N.A F. virilis 10.127 0.003 2 48 N.A N.A 12.788 < 0.001 2 40 F 6.471 0.018 1 22 N.A N.A 9.330 0.005 1 19 M 4.246 0.097 2 26 N.A N.A 3.179 0.236 2 21 P. acutus 0.862 0.854 2 36 4.210 0.127 2 41 0.729 0.824 2 43 N.A F 2.742 0.405 2 23 2.229 0.432 2 22 3.207 0.244 2 23 N.A M 0.325 0.510 1 13 2.701 0.404 2 19 0.586 0.392 2 20 N.A P. clarkii 1.262 1.000 2 36 7.553 0.014 2 37 11.920 0.001 2 36 N.A F 1.023 1.000 2 20 3.024 0.366 2 23 5.927 0.025 2 21 N.A M Constant 5.091 0.055 1 14 7.645 0.007 2 15 N.A F females, M males, N.A. not tested at all, N.D. no data available because all specimens from one sex escaped during the acclimatiza- tion period constant: exactly the same response in treatment and control Treatments that significantly (p ≤ 0.05) deviated from control are in bold and italic and trends (0.05 < p ≤ 0.10) in bold only and match sizes of occupied burrows in field obser - present study might be underestimated for the spring/ vations (Souty-Grosset et  al. 2014). The number of early season. burrows dug by crayfish has been related to type and Burrowing behaviour has also been linked to the composition of the sediment (Stanton 2004; Emery- reproductive cycle (Romaire and Lutz 1989; Hold- Butcher et  al. 2023). The foam used in this study ich and Black 2007) and especially to females with does not resemble natural sediments at all, and may eggs retreating in burrows (Hasiotis 1995). To avoid therefore have affected the burrowing behaviour of bias in the results due to a few gravid females, these the tested species. However, all species showed to be specimens were excluded from the experiment. The able to remove the foam from the pipe and occupy the different runs for each species were performed within pipe in at least one of the treatments and, therefore, a relatively short period of time and by that excluding the general set-up is regarded suitable as a means to seasonal variation. The advantage of this approach study burrowing behaviour in a standardized way. is that significant differences among treatments are The various species were tested in spring/early sum- indeed due to the applied triggers and thus shed light mer in different years, except for P. leniusculus that on how each species responds to the triggers applied. was tested in autumn/early winter. Since activity of P. The responses, however, may change over the seasons leniusculus shows a seasonal cycle with low activity and repeating the experiments in other seasons may in winter (Flint 1977), their burrowing activity in the reveal the consistency in response to the triggers. Vol.: (0123456789) 1 3 Aquat Ecol Vol:. (1234567890) 1 3 Table 5 Results of Fisher’s exact tests to evaluate differences in response among species to the treatments Treatment Fisher’s exact test Behaviour Species χ2 p df n A. astacus P. leptodactylus P. leniusculus F. limosus F. virilis P. acutus P. clarkii Control 86.836 < 0.001 12 187 Burrow 5.1 -0.4 0.2 -2.2 4.7 −3.7 −4.3 Escape − 1.2 − 1.2 0.2 − 0.2 − 1.2 4 − 0.2 No Response − 4.6 0.9 − 0.3 2.3 − 4.1 1.9 4.3 Shelter 45.319 < 0.001 12 148 Burrow 3.4 1.8 0 − 3.5 2.3 − 2.1 − 2.6 Escape 0.2 − 1.1 1 − 1.1 0 1.9 − 0.8 No Response − 3.4 − 1.3 − 0.5 3.9 − 2.2 1.2 2.9 Increased light intensity 29.734 < 0.001 8 80 Burrow 3.8 0.1 − 3.7 0.3 0.7 Escape N.T − 0.8 1.3 − 1.4 N.T 0.8 0.1 No Response − 3.3 − 0.7 4.2 − 0.7 − 0.7 Increased water temperature 16.48 0.017 8 72 Burrow 2.2 − 1 − 1.9 − 1 1.6 Escape N.T − 1.6 − 0.6 − 1.2 N.T 1.7 1.1 No Response − 1 1.3 2.6 − 0.2 − 2.2 Increased crayfish density 37.024 < 0.001 6 88 Burrow 1.9 − 0.3 − 2.6 1 Escape − 1.8 − 1.6 − 1.7 N.T 5.8 N.T N.T No Response − 0.9 1.1 3.4 − 4.2 Test results (Chi-square, p value, degree of freedom, total observations) are given as well as the standardized residuals. Significant standardized residuals are in bold and italic. Positive values indicate more frequently observed and negative values less frequently observed N.T. species not tested Aquat Ecol Crayfish use refuge and burrows to be pro- females in burrow activity prior to mating and Ber- tected against predators, to withstand environmental rill and Chenoweth (1982) also found no differences extremes or for reproduction (Hobbs 1981; Barbaresi between sexes. On the other hand, the study of Guo et al. 2004; Stoeckel et al. 2011). Excavating burrows et  al. (2020) indicated that there were differences by crayfish seem to be inversely linked to the avail- between female and male P. clarkii in shelter use also ability of natural shelters present (Berrill and Che- outside the reproductive period. In the present study, noweth 1982; Ilhéu et  al. 2003). When no shelter in which no gravid females were used, most treatment was present in our experiment, certain species show and species combinations did not show sex-specific active burrowing behaviour (A. astacus, F. virilis, P. responses and thus supports the lack of differences in leptodactylus), while others show hardly any bur- burrowing behaviour between males and females. rowing activity (P. clarkii, male F. limosus), limited Crayfish use natural refuges besides burrows to burrowing activity (female F. limosus, P. leniusculus) seek shelter and the presence of natural shelters seem or only limited escape behaviour (P. acutus). In per- to reduce burrowing activity (Flint 1975; Ilhéu et  al. manent water with similar environmental laboratory 2003; Groza et  al. 2016). The observations in the conditions, the examined crayfish species thus differ present study showed that the presence of a shelter in their burrowing response. Our laboratory findings indeed reduced burrowing behaviour in A. astacus, F. therefore, support the field observations that among limosus, and F. virilis. Interestingly, the presence or crayfish that live in open water some species burrow absence of a shelter did not lead to a change in their and others not depending on the prevailing conditions behaviour of P. leniusculus, P. leptodactylus, P. acu- (Berrill and Chenoweth 1982). This burrowing capa- tus and P. clarkii. Remarkably, for F. limosus, lack of bility seems, however, to be flexible since P. lenius- shelter was the only environmental stressor that trig- culus, which is considered a non-burrowing species, gered burrowing behaviour. According to the results heavily burrowed outside its native range in the banks of the present study, the response to shelter availabil- of a river in the UK (Guan 1994) and also showed ity is likely to be species-specific. burrowing behaviour in our study. Similarly, Kaestner Crayfish species vary in their ability to survive out (1991) and Statzner et al. (2000) mention that F. limo- of water (Reynolds et al. 2012; Kouba et al. 2016) and sus does not burrow while other sources e.g. Holdich one way to deal with desiccation is excavating bur- and Black (2007) state this species is a notorious bur- rows (Hobbs 1981; Peay and Dunn 2014). A decrease rower. Even among genetically uniform specimens, in water level may induce burrowing activity as behavioural plasticity in burrowing has been observed observed in P. clarkii by Correia and Ferreira (1995) (Linzmaier et al. 2018). and both increasing water temperature and increas- The present study observed that there were sig- ing light availability may act as early warning signals nificant differences in burrowing activity between for upcoming lower water levels (Boulton 2003). The females and males from the same species, with, for burrowing behaviour of P. clarkii has been related to example, less P. leptodactylus males burrowing com- drought avoidance (Hobbs 1981), and in the present pared to females when a shelter was present. Signifi- study P. clarkii was the only species that increased cant differences between sexes were also found for burrowing activity to both drought indicators. The P. acutus in the increased water temperature treat- response of P. clarkii was stronger to the water tem- ment and for P. leniusculus for the increased density perature increase than the light intensity increase with treatment. Especially during sensitive life history more specimens burrowing at higher water tempera- phases, use of shelters by crayfish is of great impor - tures. Pontastacus leptodactylus also increased bur- tance (Barbaresi et  al. 2004; Stoeckel et  al. 2011). rowing activity at increased light intensity but not For example, P. clarkii maternal females showed a with higher water temperatures which is in line with much stronger shelter competition and use than con- the observation by Valido et al. (2021). Interestingly, specific males or non-maternal females (Figler et  al. both drought triggers caused a total lack of response 2001; Haubrock et  al. 2019) and such shelter-related in F. limosus. This species generally occurs in all aggression seems to be quite common in decapods types of water bodies but prefers warmer, slow-flow - (Figler et  al. 1998). In addition, Haubrock et  al. ing and standing waters and is very tolerant to a vari- (2019) observed no differences between males and ety of environmental stressors and this high tolerance Vol.: (0123456789) 1 3 Aquat Ecol towards eutrophic conditions and water temperature managing crayfish populations and the problems they may explain the observed lack of response (Todorov cause. Like in many countries in Europe (e.g. Kouba et  al. 2020). Crayfish are in general night-active and et  al. 2014; Souty-Grosset et  al. 2016), the Nether- search more actively for shelter (Flint 1975, 1977) lands has to deal with several invasive crayfish spe- and occupy more shelters during day compared to cies (Lemmers et al. 2021; van Kuijk et al. 2021). The the night (Ranta and Lindström 2010; Thomas et  al. presence of these burrowing animals may increase 2016). Furthermore, increased artificial light during the risk of bank erosion (Harvey et al. 2019) resulting the night increased the time P. leniusculus spent in in concerns of dike collapses in peatland areas in the the shelter (Thomas et  al. 2016). Nevertheless, this Netherlands (Lemmers et al. 2021). High burrow den- study clearly indicate that the responses to drought sity by P. leniusculus had led to considerable damage triggers are species-specific. of river banks in the UK (Guan 1994) and burrow- The density treatment in this study could only be ing activity by P. clarkii in rice field dikes in Portugal applied to a limited number of species and gave inter- resulted in leakages and finally the collapse of these esting results. The response to this treatment seems delimiting banks (Fonseca et al. 1997; Holdich 1999). also species-specific with A. astacus and P. leniuscu- The most widespread invasive crayfish species in the lus showing less burrowing, P. leptodactylus having Netherlands are F. limosus and P. clarkii (van Kuijk no change in behaviour and F. virilis showing a larger et al. 2021). The present study showed that F. limosus proportion of specimens trying to escape. Studies greatly lowers burrowing activity when natural shel- have indicated that the number of burrows is uncor- ters are present. The Netherlands has an extensive and related with crayfish density (Guan 1994; Ilhéu et al. complex network of ditches and canals to discharge 2003; Haubrock et  al. 2019) and this seems to con- excess water (Verdonschot et  al. 2011). The sedi- tradict the results from this study except for P. lep- ment in those ditches and canals frequently consists todactylus. Unlike in field conditions where multiple of fine material and thus ideal for crayfish to burrow opportunities are present, there was only one place (Correia and Ferreira 1995; Barbaresi et  al. 2004). where the animals could dig a burrow in the present Intense management of these systems through fre- study. The lower burrowing activity of A. astacus and quent dredging and yearly thoroughly cleaning of the P. leniusculus could possibly be due to specimens vegetation in the water ways has resulted in a homo- interacting more with the other specimen present in geneous underwater environment. The lack of shelters the experimental arena than seeking shelter. Support in those environments is probably one of the most for this hypothesis comes from observations that dif- important triggers for F. limosus to burrow. Chang- ferences in levels of aggression determine access to ing the way of managing water courses and creating a limited shelter together with fighting constituting a more heterogeneous environment with more variabil- high proportion of total interactions in equally sized ity in natural shelters might help to refrain F. limosus pairs (Vorburger and Ribi 1999). An alternative from burrowing. explanation for the unoccupied shelters could be that The lack of shelters does not seem to be an the dominant crayfish prevented the subordinate one important trigger to burrow for the other wide- from using it. This was also observed by Gherardi and spread species P. clarkii in the Netherlands as dem- Daniels (2004) in an interspecies shelter occupancy onstrated in the control treatment of the present experiment where the dominant P. clarkii did not use experiment. Although the species did not burrow the shelter after evicting subordinate P. acutus acutus in ephemeral waters in Portugal, it did make use of from it. Unfortunately, no video recordings have been boulders and complex microhabitats in the wild to made in the present study to verify this. shelter (Aquiloni et  al. 2005). It might be valuable to investigate if adding complex habitats in other- Implications wise homogeneous environments may lower bur- rowing intensity of this species. In the present The results of the present experiments indicate study, P. clarkii clearly responded to the increased that the tested species showed a different burrow - water temperature which is in line with studies indi- ing response to the triggers they were exposed to. cating that crayfish demonstrated greater burrowing These species-specific responses are very relevant for activity with higher water temperatures (Flint 1977; Vol:. (1234567890) 1 3 Aquat Ecol Acknowledgements Many thanks to Rene van Wijgaarden Guan and Wiles 1997; Bubb et  al. 2002; Stanton and Jelle Touwen for their help with catching crayfish (P. leni- 2004). Although Ilhéu et  al. (2003) found no rela- usculus). We are grateful to two anonymous reviewers for their tionship between total burrow density and P. clarkii valuable comments. population size, the number of active burrows has Authors contribution EP: conceptualization, methodology, been positively correlated with the density of P. verification, formal analysis, visualization, supervision, writ- clarkii (Arce and Diéguez-Uribeondo 2015). Inter- ing—original draft. RV: investigation, verification, formal anal- estingly, P. clarkii seems to be an inefficient user ysis, visualization, writing—original draft. JE: investigation, of its burrows as Barbaresi et  al. (2004) found that methodology, writing—review and editing. ML: investigation, writing—review and editing. RH: investigation, writing— individuals stayed on average 6  h in a burrow and review and editing. IR: conceptualization, methodology, veri- once abandoned, they started excavating a new bur- fication, resources, supervision, writing—review and editing. row instead of reoccupying the old one in areas with dense P. clarkii populations. The inefficient use Data availability The data underlying this study are included of burrows in combination with warmer summers in the published article and can be found in Online Resource 2. due to climate change may lead to large amounts Declarations of removed bank sediments and possibly to col- lapses of dikes. For water managers, more insight is Conflict of interest All authors declare to have no competing needed in how to prevent such massive burrowing. interests. More knowledge on how to reduce burrowing activ- Open Access This article is licensed under a Creative Com- ity as well as more knowledge of factors governing mons Attribution 4.0 International License, which permits P. clarkii population dynamics are essential for a use, sharing, adaptation, distribution and reproduction in any proper managing these invaders. medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Crea- tive Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated Conclusion otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds In conclusion, the present experiment shows that bur- the permitted use, you will need to obtain permission directly rowing behaviour among freshwater crayfish is spe- from the copyright holder. To view a copy of this licence, visit cies-specific and for some species sex specific. This http:// creat iveco mmons. org/ licen ses/ by/4. 0/. study also shed light on how crayfish will alter their burrowing behaviour in response to climate change. Droughts are likely to increase in certain areas in the world, and our results show that early warning signals References of drought increase burrowing behaviour for certain Albertson LK, Daniels MD (2018) Crayfish ecosystem engi- species. The response to burrowing triggers is spe- neering effects on riverbed disturbance and topography cies-specific with lack of shelter as a strong driver to are mediated by size and behavior. Freshw Sci 37:836– burrow for A. astacus, F. limosus and F. virilis, while 844. https:// doi. org/ 10. 1086/ 700884 increased light intensity triggers burrowing behaviour Aquiloni L, Ilhéu M, Gherardi F (2005) Habitat use and disper- sal of the invasive crayfish Procambarus clarkii in ephem- in P. leptodactylus, P. acutus and P. clarkii and low- eral water bodies of Portugal. Mar Freshw Behav Physiol ered activity of F. limosus. Increased water tempera- 38:225–236. https:// doi. org/ 10. 1080/ 10236 24050 03101 95 ture was the most important trigger for P. clarkii to Arce JA, Diéguez-Uribeondo J (2015) Structural damage burrow. The presence of a conspecific reduced bur - caused by the invasive crayfish Procambarus clarkii (Girard, 1852) in rice fields of the Iberian Peninsula: a rowing activity in A. astacus and P. leniusculus and study case. Fund Appl Limnol 186:259–269. https:// doi. triggered F. virilis to escape. Testing in a field situa- org/ 10. 1127/ fal/ 2015/ 0715 tion whether more complex habitats indeed result in Barbaresi S, Gherardi F (2006) Experimental evidence for lower burrowing activity together with more knowl- homing in the red swamp crayfish, Procambarus clarkii. Bull Fr Pêche Piscic 380–381:1145–1154. https:// doi. org/ edge on the causes of the species-specific responses 10. 1051/ kmae: 20060 17 and population dynamics may help managing popula- tions of these invasive species. Vol.: (0123456789) 1 3 Aquat Ecol Flint RW (1977) Seasonal activity, migration and distribution Barbaresi S, Tricarico E, Gherardi F (2004) Factors inducing of the crayfish, Pacifastacus Ieniusculus, in Lake Tahoe. the intense burrowing activity of the red-swamp cray- Am Midl Nat 97:280–292. https:// doi. org/ 10. 2307/ 24250 fish, Procambarus clarkii, an invasive species. Natur- wissenschaften 91:342–345. https:// doi. org/ 10. 1007/ Florey CL, Moore PA (2019) Analysis and description of bur- s00114- 004- 0533-9 row structure in four species of freshwater crayfishes Berrill M, Chenoweth B (1982) The burrowing ability of non- (Decapoda: Astacoidea: Cambaridae) using photogram- burrowing crayfish. Am Midl Nat 108:199–201. https:// metry to recreate casts as 3D models. J Crustac Biol doi. org/ 10. 2307/ 24253 10 39:711–719. https:// doi. org/ 10. 1093/ jcbiol/ ruz075 Boulton AJ (2003) Parallels and contrasts in the effects of Fonseca JC, Marques JC, Madeira VMC (1997) Oxygen uptake drought on stream macroinvertebrate assemblages. Freshw inhibition in Procambarus clarkii, red swamp crayfish, Biol 48:1173–1185. https:// doi. org/ 10. 1046/j. 1365- 2427. by biogradable surfactants: an ecotechnological approach 2003. 01084.x for population control in rice fields. Freshw Crayfish Bubb DH, Lucas MC, Thom TJ (2002) Winter movements 11:235–242 and activity of signal crayfish Pacifastacus leniusculus Gherardi F, Daniels WH (2003) Dominance hierarchies and in an upland river, determined by radio telemetry. Hyd- status recognition in the crayfish Procambarus acutus robiologia 483:111–119. https:// doi. org/ 10. 1023/A: 10213 acutus. Can J Zool 81:1269–1281. https:// doi. org/ 10. 63109 155 1139/ z03- 107 Burras L, Blakewood G, Richard T, Huner JV (1995) Labora- Groza MI, Pop-Vancia V, Mireşan V (2016) Diel activity and tory observations on burrowing in different soils by com- use of multiple artificially constructed shelters in Astacus mercially important procambarid crayfish. Freshw Cray - leptodactylus (Decapoda: Astacidae). Biologia 71:1369– fish 10:427–434 1379. https:// doi. org/ 10. 1515/ biolog- 2016- 0167 Correia AM, Anastácio PM (2008) Shifts in aquatic macroin- Guan RZ (1994) Burrowing behaviour of signal crayfish, Paci- vertebrate biodiversity associated with the presence and fastacus leniusculus (Dana), in the river Great Ouse, Eng- size of an alien crayfish. Ecol Res 23:729–734. https:// doi. land. Freshwater Forum 4:144–168 org/ 10. 1007/ s11284- 007- 0433-5 Guan RZ, Wiles P (1997) The home range of signal crayfish in Correia AM, Ferreira O (1995) Burrowing behavior of the a British lowland river. Freshwater Forum 8:45–54 introduced red swamp crayfish Procambarus clarkii Guo W, Hossain MS, Kubec J et al (2020) Psychoactive com- (Decapoda: Cambaridae) in Portugal. J Crustacean Biol pounds at environmental concentration alter burrowing 15:248–257. https:// doi. org/ 10. 2307/ 15489 53 behavior in the freshwater crayfish. Sci Total Environ Crandall KA, De Grave S (2017) An updated classification of 711:135138. https:// doi. org/ 10. 1016/j. scito tenv. 2019. the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list. J Crustacean Biol Harvey GL, Henshaw AJ, Brasington J, England J (2019) Bur- 37:615–653. https:// doi. org/ 10. 1093/ jcbiol/ rux070 rowing invasive species: an unquantified erosion risk at Emery-Butcher HE, Beatty SJ, Robson BJ (2023) Seasonal and the aquatic-terrestrial interface. Rev Geophys 57:1018– perennial water populations of an endemic crayfish differ 1036. https:// doi. org/ 10. 1029/ 2018R G0006 35 in behavioural responses to drying but not metabolism. Hasiotis ST (1995) Notes on the burrow morphologies and Ecohydrology. https:// doi. org/ 10. 1002/ eco. 2566 Faller M, Harvey GL, Henshaw AJ et al (2016) River bank bur- nesting behaviors of adults and juveniles of Procambarus rowing by invasive crayfish: spatial distribution, biophysi- clarkii and Procambarus acutus acutus (Decapoda: Cam- cal controls and biogeomorphic significance. Sci Total baridae). Freshw Crayfish 8:623–634. https:// doi. org/ 10. Environ 569–570:1190–1200. https:// doi. org/ 10. 1016/j. 5869/ fc. 1995. v8. 623 scito tenv. 2016. 06. 194 Haubrock PJ, Inghilesi AF, Mazza G et  al (2019) Burrow- Fernández-De-Miguel F, Aréchiga H (1992) Sensory inputs ing activity of Procambarus clarkii on levees: analys- mediating two opposite behavioural responses to light in ing behaviour and burrow structure. Wetl Ecol Manag the crayfish Procambarus clarkii. J Exp B 164:153–169. 27:497–511. https:// doi. org/ 10. 1007/ s11273- 019- 09674-3 https:// doi. org/ 10. 1242/ jeb. 164.1. 153 Hobbs HH (1981) The crayfishes of Georgia. Smithson Contrib Field A (2013) Discovering statistics using IBM SPSS statis- Zool. https:// doi. org/ 10. 5479/ si. 00810 282. 318 tics, 4th edn. SAGE Publications, London Holdich DM (1999) The negative effects of established crayfish Figler MH, Peeke HVS, Chang ES (1998) Shelter-related introductions. In: Gherardi F (ed) Crayfish in Europe as aggression between adult male conspecific intruders and Alien Species, 1st edn. Routledge, Milton Park, pp 31–47. resident maternal American lobsters (Homarus ameri-https:// doi. org/ 10. 1201/ 97813 15140 469 canus) with eggs at different stages of embryogenesis. Holdich D, Black J (2007) The spiny-cheek crayfish, Mar Freshw Behav Physiol 31:151–166. https:// doi. org/ Orconectes limosus (Rafinesque, 1817) [Crustacea: 10. 1080/ 10236 24980 93870 70 Decapoda: Cambaridae], digs into the UK. Aquat Inva- Figler MH, Blank GS, Peeke HVS (2001) Maternal territorial- sions 2:1–15. https:// doi. org/ 10. 3391/ ai. 2007.2. 1.1 ity as an offspring defense strategy in red swamp crayfish Ilhéu M, Acquistapace P, Benvenuto C, Gherardi F (2003) (Procambarus clarkii, Girard). Aggress Behav 27:391– Shelter use of the red-swamp crayfish (Procambarus 403. https:// doi. org/ 10. 1002/ ab. 1024 clarkii) in dry-season stream pools. Arch Hydrobiol Flint RW (1975) The natural history, ecology and production 157:535–546. https:// doi. org/ 10. 1127/ 0003- 9136/ 2003/ of the crayfish, Pacifastacus leniusculus, in a subalpine 0157- 0535 lacustrine environment. University of California, Davis Vol:. (1234567890) 1 3 Aquat Ecol Netherlands. Aquat Invasions 12:397–404. https:// doi. org/ Kaestner A (1991) Lehrbuch der Speziellen Zoologie. Band I. 10. 3391/ ai. 2017. 12.3. 12 Wirbellose. 2. Teil. Crustacea. Fisher Romaire RP, Lutz CG (1989) Population dynamics of Pro- Kouba A, Petrusek A, Kozak P (2014) Continental-wide dis- cambarus clarkii (Girard) and Procambarus acutus acu- tribution of crayfish species in Europe: update and maps. tus (Girard) (Decapoda: Cambaridae) in commercial Knowl Manag Aquat Ec 413:05. https:// doi. org/ 10. 1051/ ponds. Aquaculture 81:253–274. https:// doi. org/ 10. 1016/ kmae/ 201400 0044- 8486(89) 90151-8 Kouba A, Tíkal J, Císař P et  al (2016) The significance of Sanders H, Rice SP, Wood PJ (2021) Signal crayfish burrow - droughts for hyporheic dwellers: evidence from freshwater ing, bank retreat and sediment supply to rivers: a biophys- crayfish. Sci Rep 6:26569. https:// doi. org/ 10. 1038/ srep2 ical sediment budget. Earth Surf Process Landf 46:837– 852. https:// doi. org/ 10. 1002/ esp. 5070 Lemmers P, Collas F, Gylstra R et  al (2021) Risks and man- Souty-Grosset C, Reynolds J, Gherardi F et al (2014) Burrow- agement of alien freshwater crayfish species in the Rhine- ing activity of the invasive red swamp crayfish, Procamb- Meuse river district. Manag Biol Invasions 12:193–220. arus clarkii, in fishponds of la Brenne (France). Ethol https:// doi. org/ 10. 3391/ mbi. 2021. 12.1. 13 Ecol Evol 26:263–276. https:// doi. org/ 10. 1080/ 03949 370. Linzmaier SM, Goebel LS, Ruland F, Jeschke JM (2018) 2014. 892538 Behavioral differences in an over-invasion scenario: Souty-Grosset C, Anastácio PM, Aquiloni L et  al (2016) The marbled vs. spiny-cheek crayfish. Ecosphere 9:e02385. red swamp crayfish Procambarus clarkii in Europe: https:// doi. org/ 10. 1002/ ecs2. 2385 impacts on aquatic ecosystems and human well-being. McClain WR (2013) Effects of simulated precipitation Limnologica 58:78–93. https:// doi. org/ 10. 1016/j. limno. extremes on crayfish (Procambarus clarkii Girard) ovi- 2016. 03. 003 position in artificial burrows. Aquac Res 44:612–617. Stanton JA (2004) Burrowing behaviour and movements of the https:// doi. org/ 10. 1111/j. 1365- 2109. 2011. 03066.x signal crayfish Pacifastacus leniusculus (Dana). Thesis, Mojžišová M, Mrugała A, Kozubíková-Balcarová E et  al University of Leicester (2020) Crayfish plague in Czechia: outbreaks from Statzner B, Fièvet E, Champagne J-Y et  al (2000) Crayfish as novel sources and testing for chronic infections. J Inver- geomorphic agents and ecosystem engineers: biological tebr Pathol 173:107390. https:// doi. org/ 10. 1016/j. jip. behavior affects sand and gravel erosion in experimental 2020. 107390 streams. Limnol Oceanogr 45:1030–1040. https:// doi. org/ Mojžišová M, Svobodová J, Kozubíková-Balcarová E et  al 10. 4319/ lo. 2000. 45.5. 1030 (2022) Long-term changes in the prevalence of the Statzner B, Peltret O, Tomanova S (2003) Crayfish as geomor - crayfish plague pathogen and its genotyping in inva- phic agents and ecosystem engineers: effect of a biomass sive crayfish species in Czechia. NeoBiota 74:105–127. gradient on baseflow and flood-induced transport of gravel https:// doi. org/ 10. 3897/ NEOBI OTA. 74. 79087 and sand in experimental streams. Freshw Biol 48:147– Nystrom P, Strand JA (1996) Grazing by a native and an 163. https:// doi. org/ 10. 1046/j. 1365- 2427. 2003. 00984.x exotic crayfish on aquatic macrophytes. Freshw Biol Stoeckel JA, Helms BS, Cash E (2011) Evaluation of a crayfish 36:673–682. https:// doi. org/ 10. 1046/j. 1365- 2427. 1996. burrowing chamber design with simulated groundwater d01- 508.x flow. J Crustacean Biol 31:50–58. https:// doi. org/ 10. 1651/ Nystrom P, Bronmark C, Graneli W (1999) Influence of an exotic and a native crayfish species on a littoral benthic 09- 3271.1 community. Oikos 85:545. https:// doi. org/ 10. 2307/ 35467 Suzuki T, Arikawa K, Eguchi E (1985) The effects of light and 04 temperature on rhodopsin-porphyropsin visual system of Payette AL, McGaw IJ (2003) Thermoregulatory behavior of the crayfish, Procambarus clarkii. Zoolog Sci 2:455–461 the crayfish Procambarus clarki in a burrow environment. Thomas JR, James J, Newman RC et  al (2016) The impact of Comp Biochem Phys A 136:539–556. https:// doi. org/ 10. streetlights on an aquatic invasive species: artificial light 1016/ S1095- 6433(03) 00203-4 at night alters signal crayfish behaviour. Appl Anim Behav Peay S, Dunn AM (2014) The behavioural response of the Sci 176:143–149. https:// doi. org/ 10. 1016/j. appla nim. invasive signal crayfish Pacifastacus leniusculus to 2015. 11. 020 experimental dewatering of burrows and its implications Tilmans M, Mrugała A, Svoboda J et  al (2014) Survey of the for eradication treatment and management of ponds with crayfish plague pathogen presence in the Netherlands crayfish. Ethol Ecol Evol 26:277–298. https:// doi. org/ 10. reveals a new Aphanomyces astaci carrier. J Invertebr 1080/ 03949 370. 2014. 903379 Pathol 120:74–79. https:// doi. org/ 10. 1016/j. jip. 2014. 06. Ranta E, Lindström K (2010) Power to hold sheltering burrows 002 by juveniles of the signal crayfish, Pasifastacus leniuscu- Todorov M, Trichkova T, Hubenov Z, Jurajda P (2020) Faxo- lus. Ethology 92:217–226. https:// doi. org/ 10. 1111/j. 1439- nius limosus (Rafinesque, 1817) (Decapoda: Cambaridae), 0310. 1992. tb009 61.x a new invasive alien species of European Union concern Reynolds J, Souty-Grosset C, Richardson A (2012) Crayfish in Bulgaria. Acta Zool Bulgar 72:113–121 as prime players in ecosystems: life-history strategies. In: Valido CAR, Johnson MF, Dugdale SJ et  al (2021) Thermal Reynolds J, Souty-Grosset C (eds) Management of fresh- sensitivity of feeding and burrowing activity of an inva- water biodiversity: crayfish as bioindicators. Cambridge sive crayfish in UK waters. Ecohydrology 14:e2258. University Press, Cambridge, pp 59–82https:// doi. org/ 10. 1002/ eco. 2258 Roessink I, Gylstra R, Heuts P et al (2017) Impact of invasive van Kuijk T, Biesmeijer JC, van der Hoorn BB, Verdonschot crayfish on water quality and aquatic macrophytes in the PFM (2021) Functional traits explain crayfish invasive Vol.: (0123456789) 1 3 Aquat Ecol success in the Netherlands. Sci Rep 11:2772. https:// doi. Weber S, Traunspurger W (2017) Invasive red swamp crayfish org/ 10. 1038/ s41598- 021- 82302-4 (Procambarus clarkii) and native noble crayfish (Astacus Verdonschot RCM, Keizer-vlek HE, Verdonschot PFM (2011) astacus) similarly reduce oligochaetes, epipelic algae, Biodiversity value of agricultural drainage ditches: a and meiofauna biomass: a microcosm study. Freshw Sci comparative analysis of the aquatic invertebrate fauna 36:103–112. https:// doi. org/ 10. 1086/ 690556 of ditches and small lakes. Aquat Conserv 21:715–727. https:// doi. org/ 10. 1002/ aqc. 1220 Publisher’s Note Springer Nature remains neutral with regard to Vorburger C, Ribi G (1999) Aggression and competition for jurisdictional claims in published maps and institutional affiliations. shelter between a native and an introduced crayfish in Europe. Freshw Biol 42:111–119. https:// doi. org/ 10. 1046/j. 1365- 2427. 1999. 00465.x Vol:. (1234567890) 1 3

Journal

Aquatic Ecology – Springer Journals

Published: Sep 14, 2023

Keywords: Density; Invasive species; Light intensity; Shelter; Water temperature

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