Many animals fight over a limited valuable resource. In marmorkrebs (marbled crayfish), large animals usually defeat small opponents but they are frequently beaten by small opponents that are shelter owners. A prior residence effect of marbled crayfish was analysed quantitatively in the present study. More than 2 h of residency in a shelter was sufficient for small owners to defeat large intruders. Small animals that stayed in a shelter for 24 h still tended to win following removal of the shelter 10 min before pairing with large intruders, but 2 h residents were occasionally beaten by large intruders without the support of shelters during pairings. The prior residence effect thus developed depending on the duration of residency. To clarify whether the strength of the prior residence effect was affected by the quality of a shelter, large and small owners with different combinations of high- and low-quality shelters were paired. When both large and small owners possessed a high-quality shelter, the frequency of agonistic bouts was reduced. Even if agonistic bouts occurred, the win frequency of small owners was almost equal to that of large owners. Thus, the residence effect on small owners was sufficiently strong to overcome the physical disadvantage of small animals to large opponents. By contrast, small owners of low­-quality shelters were frequently beaten by large owners with the shelters of same or better quality. We conclude that the outcome of fights over the resource shelter is highly dependent on both the perception of shelter quality and body size differences.

For many animals, the acquisition of an adequate shelter reduces the risk of predation and increases their survival. A shelter is thus a valuable resource for animals and induces intraspecific competition for occupation. Lower ranked animals are found to occupy and defend shelters less frequently than dominant animals (Fero and Moore, 2014). Shelter possession therefore is, in part, mediated by the social status of an animal. For agonistic encounters, larger sized animals or animals with larger weapons have a physical advantage and tend to win encounters in both vertebrates and invertebrates (e.g. Clutton-Brock et al., 1979; Tokarz, 1985; Ueno and Nagayama, 2012). The outcome of agonistic bouts also affects subsequent fights. Known as ‘winner and loser effects’, winning animals are more likely to win their next fight while losing animals are more likely to lose (Hsu et al., 2006; Momohara et al., 2013). A similar experience factor that affects intraspecific competition is known as a ‘prior residence effect’, in which residents have a greater likelihood of dominating intruders or newcomers (Braddock, 1949). A prior residence effect is found in mammals including humans, birds, fish, frogs and insects (Davies, 1978; Baugh and Forester, 1994; Huntingford and Leaniz, 1997; Faria et al., 1998; Snell-Rood and Cristol, 2005; Han et al., 2009; Nijman and Heuts, 2011). This effect has also been reported in various decapod crustaceans, including lobsters (Karnofsky et al., 1989), prawns (Evans and Shehadi-Moacdieh, 1988), fiddler crabs (Hyatt and Salmon, 1978) and crayfish (Peeke et al., 1995; Figler et al., 1999, 2005; Herberholz et al., 2007; Klar and Crowley, 2012).

Many animals have their own preferred shelters. The quality of a shelter strongly affects the strength of the prior residence effect. In spiders (Riechert, 1979) and fish (Nijman and Heuts, 2000), territorial owners exhibit higher defence performance for preferred high-quality habitats than for poor habitats. In young brown trout, owners of more preferred habitats attack intruders sooner than owners of less preferred habitats, and more satisfied owners are more aggressive relative to intruders (Johnsson et al., 2000). Vance (1972) also demonstrated that the adequacy of the hermit crab shell affects the probability of winning agonistic bouts. Thus, animals adjust their fighting behaviour when the resource value is changed. The cost of fighting will increase when the quality of a shelter increases, and the probability of victory for an animal will increase when the resource value is increased only to that animal (Enquist and Leimar, 1987). In contrast, Gherardi (2006) found that hermit crabs with low-quality shells are more motivated to fight, and take risks, than crabs in better-fitting shells. There are, however, no quantitative systematic analyses that clarify the interactions between the quality of a shelter and the agonistic encounters over shelter ownership.

In this study, we characterized the dependence of the prior residence effect of marmorkrebs (marbled crayfish) on shelter quality. Marmorkrebs are thought to be a parthenogenetic form of Procambarus fallax (Scholtz et al., 2003; Martin et al., 2007) and/or Procambarus virginalis (Vogt et al., 2015). They produce genetically uniform clones and their central nervous system is probably similar to that of Procambarusclarkii (Faulkes, 2016), in which agonistic interactions and winner/loser effects have been well studied (Fujimoto et al., 2011; Sato and Nagayama, 2012; Momohara et al., 2016, 2018; Araki et al., 2013). Their behavioural plasticity and its neurochemical basis are well characterized (Kasuya and Nagayama, 2016; Shiratori et al., 2017). They also show a strong preference for shelter selection (Takahashi and Nagayama, 2016). We confirmed the prior residence effect of small owners, and then analysed the effects of shelter quality on agonistic encounters using various combinations of different shelters with large and small animals.

Animals

Marmorkrebs (marbled crayfish, Procambarus virginalis from Lyko, 2017) were obtained from a laboratory population in our department. In this population, all individuals are females and are the offspring of three mothers that we acquired in 2010 from Professor Tochinai's laboratory at Hokkaido University, Japan. Marbled crayfish of 4.0–4.5 cm in body length from rostrum to telson were used for all experiments. The animals were maintained individually in separate opaque containers without shelter, under a 12 h (06:00–18:00 h light):12 h (18:00–06:00 h dark) light:dark cycle for at least 3 weeks. Each container was 23×18×8.5 cm (length×width×height) in size and filled with water to about half-depth. Each animal was fed a standard amount of small food pellets (Kyorinn, Japan) twice a week, and was last fed at least 3 days before an experiment. Crayfish that had moulted in the week prior to the start of an experiment or crayfish undergoing egg laying were not used in this study.

Experimental procedure for agonistic bouts

Experimental trials were carried out in a dimly lit laboratory at a room temperature of approximately 23°C. The day before pairing, the body length (from rostrum to telson) of each animal was measured. Two crayfish with a length difference between 3% and 7% were selected and paired in a new opaque container of 26×38×24 cm (length×width×height) filled with water to about half-depth. Prior to each trial, an opaque plastic barrier was placed in the centre of the tank, separating it into two areas. A single animal was placed on each side of this barrier and allowed to acclimate for at least 10 min before the divider was removed. PVC pipes (Mitsubishi Plastics Ltd, Tokyo, Japan) attached to the floor using Apiezon sealing compound (M&I Materials Ltd, Manchester, UK) were used as shelters. Two different pipes, 4 cm in length with a 2.6 cm internal diameter (=XL) and 2 cm in length with a 2.6 cm internal diameter (=1/2 XL) were used in this study. Two PVC pipes were usually attached longitudinally 3 cm from the centre, one on each side of the experimental container. The position and combination of the PVC pipes are shown as schematic diagrams in each figure.

The agonistic bouts of the crayfish were recorded using a video camera (GZ-MG330-S, JVC, Yokohama, Japan) mounted on a tripod above the container for 60 min. The behaviour of each crayfish was analysed using single-frame measurements to construct an ethogram of each second of the encounter. Behavioural acts that occurred during agonistic bouts were categorized as one of seven types: attack, fight, contact, approach, retreat, tailflip and neutral (Momohara et al., 2013). Change of orienting behaviour from approach to attack was an evident feature of dominant animals (Watanabe et al., 2016). We determined the establishment of dominance order in paired crayfish without shelters when the subordinate crayfish showed a retreat or tailflip following the dominant crayfish's attack at least three times in succession (Sato and Nagayama, 2012). We also determined the establishment of dominance order in paired crayfish with shelters when one of them occupied a PVC pipe.

Agonistic bouts between owner and intruder

Smaller animals (i.e. owners) were placed in the half area of the container with the XL pipe for 1, 2 or 24 h before pairing with large intruders. Intruders were placed in the other half of the container and the opaque plastic divider was removed after 10 min. In one series of experiments, the container was divided by a transparent plastic barrier and large intruders were placed in one half of the container for 24 h before being paired with small owners. Large intruders were judged as winners when they pirated a shelter from small owners, while small owners were judged as winners when they turned away intruders from their shelters.

Agonistic bouts between two owners

Both small and large animals were placed in container halves with pipe shelters (i.e. both owners) for 24 h and then paired to observe their agonistic bouts. As our previous study (Takahashi and Nagayama, 2016) showed that animals prefer the XL pipe, we observed pairings between large and small owners with different combinations of two pipes, XL and 1/2 XL, for residence effects. Animals that pirated an opponent's shelter were judged as winners. We judged draws in the case that both owners possessed their shelters after 1 h of pairing. In total, 490 animals were used in this study and each animal was used only once throughout experiments.

Statistical analyses

The win frequency was determined as: number of animals that won the pairing/total number of agonistic bouts×100 (%). The likelihood of winning between large and small animals was statistically compared between the winning number of large animals and that of small animals using a binomial test. The win frequency of small owners with different residence time was compared with that of small animals without the presence of shelters and the win frequency of large intruders with and without prior viewing of the shelter was compared with that of large animals against small animals without the presence of shelters using a Fisher's exact test. In total, we performed seven multiple comparisons with the same set of control data (pairings between naive large and naive small animals), and accordingly applied Bonferroni's correction to alpha and set the significance level to 0.007 (=0.05/7). The winning/losing number of pairings and P-value for Fisher's exact test of each treatment group against naive small or naive large animal is summarized in Table 1.

Table 1.

Summary of agonistic bouts between small owner and large intruder

Summary of agonistic bouts between small owner and large intruder
Summary of agonistic bouts between small owner and large intruder

A prior residence effect

When two marbled crayfish were paired in the container without a pipe, agonistic bouts soon started and the dominant and subordinate relationship of the two crayfish was established within 5 min. In 33 pairings between large and small crayfish in which the length difference was 3–7%, smaller crayfish won in only six pairings. The win frequency of the small animals was 18%, so larger animals had a physical advantage and tended to win. To test whether or not residency in a shelter had any effect on agonistic bouts of small crayfish, we first provided smaller animals with a shelter (XL pipe) for 1, 2 or 24 h and afterwards tested their chances of winning against large intruders (Fig. 1A). The container was divided into two areas by the opaque plastic divider and small animals were put in the half with an XL pipe for the allotted time. Crayfish moved into the pipe within 1 h. The divider was removed 10 min after the large intruder was placed into the other half of the container (inset in Fig. 1). The success rate for shelter defence from large intruders was 36% (five out of 14 pairings) for small owners that were resident for 1 h. Their win frequency was not statistically different from that of small animals without a shelter (Fisher's exact test; P=0.2628). The win frequency of small owners that were resident for 2 h was 67% (10 out of 15 pairings) and for 24 h was 68% (15 out of 22 pairings), both significantly higher than the controls without a shelter (Fisher's exact test; P=0.0021 for 2 h owners and P=0.0003 for 24 h owners). Thus, residence in a shelter for 2 h was needed to acquire a prior residence effect to overcome physical disadvantages.

Fig. 1.

Prior residence effect of small owners. (A) Win frequency of small owners that had resided in the XL shelter for 1, 2 and 24 h compared with that of small animals without a shelter (control) during agonistic bouts against large intruders. (B) Win frequency of small owners that had resided in the XL pipes for 2 or 24 h, after removal of shelters 10 min before pairing with large intruders compared with that of small animals without a shelter (same control as in A). Number of animals tested is given in parentheses. Asterisks indicate a significant difference in win frequency of small owners in comparison with control (after Fisher's exact test with Bonferroni's correction; P<0.007). Conditions of pairings are shown in the insets.

Fig. 1.

Prior residence effect of small owners. (A) Win frequency of small owners that had resided in the XL shelter for 1, 2 and 24 h compared with that of small animals without a shelter (control) during agonistic bouts against large intruders. (B) Win frequency of small owners that had resided in the XL pipes for 2 or 24 h, after removal of shelters 10 min before pairing with large intruders compared with that of small animals without a shelter (same control as in A). Number of animals tested is given in parentheses. Asterisks indicate a significant difference in win frequency of small owners in comparison with control (after Fisher's exact test with Bonferroni's correction; P<0.007). Conditions of pairings are shown in the insets.

When small owners were paired with large intruders after removal of the pipe 10 min before pairing, 67% of small owners that had resided in the XL pipe for 24 h still won (10 out of 15 pairings; Fig. 1B). The win frequency of owners that had resided in the XL pipe for 2 h, however, decreased to 40% (six out of 15 pairings). Statistically, the win frequency of 24 h owners was still significantly higher than that of the controls (Fisher's exact test; P=0.0021), but the win frequency of 2 h owners was not statistically different from the controls (Fisher's exact test; P=0.1524). Thus, as the time of residency of owners increased, the strength of the residence effect was also enhanced. The results of the statistical analyses are summarized in Table 1.

Perception of shelter by intruders

Larger animals were statistically more likely to win (27 out of 33 pairings) during agonistic bouts against small animals in the absence of a shelter (P<0.001, binomial test) (Fig. 2, control). By contrast, large intruders were frequently beaten by small owners that had been resident in the pipes for 24 h (Fig. 2, 10 min). The win frequency of large intruders was about 30% (seven out of 22 pairings), which was a statistically significant decrease from controls (Fisher's exact test, P=0.0003). In this experiment, the large intruder had little time to note the existence of a shelter on the other side of the container after removal of the divider. Thus, we divided the container with a transparent plastic barrier and large intruders were placed in the other half of the container for 24 h to allow them to observe the shelter on the other side for a long time. In this case (10 pairings), small owners defended the shelters in four pairings and large intruders seized the shelters in six pairings (Fig. 2, 24 h). Thus, the large intruders now won more frequently and there was no statistically significant difference in the win frequency from control (Fisher's exact test; P=0.2056). Therefore, this experiment revealed that the outcome of agonistic bouts was affected not only by a prior residence effect of the shelter on an owner but also the perception of the shelter existence by the intruder. As the barrier separating the tank into two areas was water permeable, chemoreception of opponents after 24 h of inhabiting the same tank could also affect agonistic motivation of both crayfish.

Fig. 2.

Win frequency of large intruders. Win frequency of large intruders with and without prior viewing of the shelter was compared with the win frequency of large animals against small animals without a shelter (control). Small owners resided in the XL pipe for 24 h before pairing and large intruders were placed in the half of the arena with the opaque plastic divider for 10 min or with the transparent plastic barrier for 24 h before pairing. Number of animals tested is given in parentheses. Asterisk indicates a significant difference in win frequency of large intruders in comparison with control (after Fisher's exact test with Bonferroni's correction; P<0.007). Conditions of pairings are shown in the insets: without prior viewing of the shelter (top) and with prior viewing of the shelter for 24 h (bottom).

Fig. 2.

Win frequency of large intruders. Win frequency of large intruders with and without prior viewing of the shelter was compared with the win frequency of large animals against small animals without a shelter (control). Small owners resided in the XL pipe for 24 h before pairing and large intruders were placed in the half of the arena with the opaque plastic divider for 10 min or with the transparent plastic barrier for 24 h before pairing. Number of animals tested is given in parentheses. Asterisk indicates a significant difference in win frequency of large intruders in comparison with control (after Fisher's exact test with Bonferroni's correction; P<0.007). Conditions of pairings are shown in the insets: without prior viewing of the shelter (top) and with prior viewing of the shelter for 24 h (bottom).

Quality of shelter affects agonistic bouts

To clarify the effects of shelter quality, both large and small animals stayed in shelters for 24 h before pairing (Fig. 3). We used the XL and the 1/2 XL pipes for shelters with various combinations of large and small owners. Both large and small animals preferred the XL pipes as the 1/2 XL pipe (2 cm length) was too short to hide the whole of the animal's body (4–4.5 cm). Animals did not stay in the 1/2 XL pipe for a long period and repeatedly entered and left the 1/2 XL pipe (Takahashi and Nagayama, 2016). When both the large and small animals were owners of XL pipes for 24 h, no contact between the two animals was observed in seven out of 17 pairings (Fig. 3A). In the remaining 10 pairings, three large animals seized the pipes from the small animals, three small animals seized the pipes from the large animals and no change of shelter possession was observed in four pairings. When one animal seized the pipe of its opponent, the winner occupied both pipes, and the loser stayed at the edge of the container with no pipes. In the pairings between large animals with the 1/2 XL pipe and small animals with the XL pipe, no contact decreased to 24% (four out of 17 pairings) and agonistic bouts for shelter possession were observed in 13 pairings (Fig. 3B). Six large owners seized the pipes from the small owners while six small owners seized the pipes from large owners. The remaining pair showed no change of shelter possession. Thus, small owners that possessed the good quality XL pipe fought an even battle with physically advantaged large owners.

Fig. 3.

Agonistic bouts between large and small owners. (A) Pairings between large and small owners with XL pipes. (B) Pairings between large owners with 1/2 XL pipes and small owners with XL pipes. (C) Pairings between large owners with XL pipes and small owners with 1/2 XL pipes. (D) Pairings between large and small owners with 1/2 XL pipes. No contact: no agonistic bouts were observed for pairings of 60 min; no change: both owners remained in their shelters for the 60 min pairing; takeover S→L: large owners seized the shelter from small owners; takeover L→S: small owners seized the shelter from large owners. Number of pairs tested is given in parentheses. Conditions of pairings are shown in the insets. *P<0.05 from binomial test.

Fig. 3.

Agonistic bouts between large and small owners. (A) Pairings between large and small owners with XL pipes. (B) Pairings between large owners with 1/2 XL pipes and small owners with XL pipes. (C) Pairings between large owners with XL pipes and small owners with 1/2 XL pipes. (D) Pairings between large and small owners with 1/2 XL pipes. No contact: no agonistic bouts were observed for pairings of 60 min; no change: both owners remained in their shelters for the 60 min pairing; takeover S→L: large owners seized the shelter from small owners; takeover L→S: small owners seized the shelter from large owners. Number of pairs tested is given in parentheses. Conditions of pairings are shown in the insets. *P<0.05 from binomial test.

In contrast, the probability that large owners seized the shelters from small owners increased in pairings between large owners with the XL pipe and small owners with the 1/2 XL pipe (Fig. 3C). Large owners won in 12 pairings while small owners won in two pairings; there was no contact in one pair. Large owners were statistically more likely to win (P<0.05, binomial test). In the case that both large and small owners resided in 1/2 XL pipes, nine large owners seized the shelters from the small owners, two small owners seized the shelters from the large owners and no change was observed in two pairings (Fig. 3D). A physical advantage of the large owners was clear in these pairings, suggesting the prior residence effect of the small owners with the lower quality shelter was weaker than that of small owners with a higher quality shelter. The win frequency of small owners with the 1/2 XL pipe (four wins and 21 defeats) decreased significantly in comparison with that of small owners with the XL pipe (nine wins and nine defeats; P<0.05, Fisher's exact test). These results strongly suggest that the strength of the prior residence effect was dependent upon shelter quality.

Evidence of residence effect

For agonistic encounters, larger animals have a physical advantage and tend to win in both vertebrates and invertebrates. In the crayfish P. clarkii, a difference of 3–7% in body length is enough for larger animals to become dominant (Ueno and Nagayama, 2012). In this study, we confirmed the physical advantage of larger marbled crayfish, and also demonstrated a prior residence effect of small crayfish. Small animals that were shelter owners frequently defeated large intruders. The win frequency of the small crayfish increased from less than 20% without a shelter to more than 65% when they resided in a shelter for more than 2 h. Animals residing in the shelter for 1 h showed no significant increase in their probability of winning.

The value asymmetry (VA) hypothesis (Johnsson and Forser, 2002) could explain why small owners often win agonistic bouts even when their fighting ability is lower than that of the large intruders. For small residents, their evaluation of the shelter increases with time, making them more motivated to defend it. The duration of residency is a critical variable in the development of the prior residence effect (Figler and Einhorn, 1983). For example, lobsters residing in an experimental tank for 24 or 48 h increase their post-threat aggressiveness, but 1 h residence has no such effect (Cromarty et al., 1999). The present study clarified that crayfish residing in the shelters for 24 h still showed high win frequencies after removal of the shelter, but crayfish residing in the shelters for 2 h did not tend to win after shelter removal. These results confirm that a prior residence effect develops depending on the duration of an animal's residency.

Residence effect depends on shelter quality

Enquist and Leimar (1987) have argued that the win probability of the shelter owners should increase with resource value, where only the owner has the opportunity of directly estimating resource value. Our results are consistent with their theoretical model. Small owners that spent much more time at the resource tended to win against large intruders that had little time to estimate resource value. The win frequency of large intruders, in contrast, increased when they observed a shelter through a transparent partition for a long period. In this case, large intruders would gain information about the resource value directly, affecting the agonistic motivation. Furthermore, the estimated quality of shelters by owners also affects the win probability. In hermit crabs, individuals in low-quality shells are more motivated to fight and take risks than crabs in better-fitting shells (Gherardi, 2006). Dowds and Elwood (1983) also observed that an attacker compares the quality of its own shell with that of its opponent and subsequently makes decisions based on this comparison. In this study, the occurrence of agonistic bouts between large and small animals was observed to reduce when both animals had preferred shelters. Furthermore, the prior residence effect of the small crayfish that acquired a higher quality shelter (the XL pipe) would be strong enough to mask their physical disadvantage in combats with large crayfish. Small animals that possessed a shelter of lower quality (the 1/2 XL pipe), by contrast, were frequently beaten by the physically advantaged larger animals with better- or same-quality shelters. Thus, the outcome of agonistic encounters over residence was strongly dependent on both the perception of shelter quality and the fighting motivation of both the owners and intruders.

Small owners residing in a shelter for 24 h tended to win after removal of the shelters. This result is similar to a winner effect that winning small animals in previous fights tend to win against large animals in the subsequent fights (Momohara et al., 2013). A decrease in cAMP level in the brain mediated by serotonin induces the winner effect (Momohara et al., 2015, 2016). At the moment, the neurochemical and physiological bases underlying the residence effect are unclear, but certain biogenic amines like serotonin could underlie this effect. In crickets, the residence effect is abolished following non-selective depletion of biogenic amines from the CNS using reserpine (Rillich et al., 2011). Further pharmacological and behavioural analyses are now required to clarify the formation and development of the prior residence effect in the marbled crayfish.

We are grateful to Prof. P. L. Newland for his critical reading of the manuscript.

Author contributions

Conceptualization: K.T., T.N.; Methodology: K.T.; Formal analysis: N.F.; Investigation: K.T., E.Y.; Data curation: N.F.; Writing - original draft: T.N.; Writing - review & editing: K.T., E.Y., N.F., T.N.; Supervision: T.N.; Funding acquisition: T.N.

Funding

This work was supported by Japanese Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology to T.N. (16K07432).

Data availability

Data supporting the results in the paper are available on request from the corresponding author (nagayama@sci.kj.yamagata-u.ac.jp).

Araki
,
M.
,
Hasegawa
,
T.
,
Komatsuda
,
S.
and
Nagayama
,
T.
(
2013
).
Social status-dependent modulation of LG-flip habituation in the crayfish
.
J. Exp. Biol.
216
,
681
-
686
.
Baugh
,
J. R.
and
Forester
,
D. C.
(
1994
).
Prior residence effect in the dart-poison frog, Dendrobates Pumilio
.
Behaviour
131
,
207
-
224
.
Braddock
,
J. C.
(
1949
).
The effect of prior residence upon dominance in the fish Platypoecilus maculatus
.
Physiol. Zool.
22
,
161
-
169
.
Clutton-Brock
,
T. H.
,
Albon
,
S. D.
,
Gibson
,
R. M.
and
Guinness
,
F. E.
(
1979
).
The logical stag: adaptive aspects of fighting in red deer (Cervus elaphus L.)
.
Anim. Behav.
27
,
211
-
225
.
Cromarty
,
S. I.
,
Mello
,
J.
and
Kass-Simon
,
G.
(
1999
).
Time in residence affects escape and agonistic behavior in adult male American lobsters
.
Biol. Bull.
196
,
105
-
112
.
Davies
,
N. B.
(
1978
).
Territorial defence in the speckled wood butterfly (Pararge aegeria): the resident always wins
.
Anim. Behav.
26
,
138
-
147
.
Dowds
,
B. M.
and
Elwood
,
R. W.
(
1983
).
Shell wars: assessment strategies and the timing of decisions in hermit crab shell fights
.
Behaviour
85
,
1
-
24
.
Enquist
,
M.
and
Leimar
,
O.
(
1987
).
Evolution of fighting behaviour: the effect of variation in resource value
.
J. Theor. Biol.
127
,
187
-
205
.
Evans
,
D. L.
and
Shehadi-Moacdieh
,
M.
(
1988
).
Body size and prior residency in staged encounters between female prawns, Palaemon elegans Rathke (Decapoda: Palaemonidae)
.
Anim. Behav.
36
,
452
-
455
.
Faria
,
C.
,
Almada
,
V.
and
Nunes
,
M. D. C.
(
1998
).
Patterns of agonistic behaviour, shelter occupation and habitat preference in juvenile Lipophrys pholis, Coryphoblennius galerita and Gobius cobitis
.
J. Fish. Biol.
53
,
1263
-
1273
.
Faulkes
,
Z.
(
2016
).
Marble crayfish as a new model organism and a new threat to native crayfish conservation
. In
Freshwater Crayfish: A Global Overview
(ed.
T.
Kawai
,
Z.
Faulkes
and
G.
Scholtz
), pp.
31
-
53
.
Boca Raton
:
CRC Press
.
Fero
,
K. C.
and
Moore
,
P. A.
(
2014
).
Shelter availability influences social behavior and habitat choice in crayfish, Orconectes virilis
.
Behaviour
151
,
103
-
123
.
Figler
,
M. H.
and
Einhorn
,
D. M.
(
1983
).
The territorial prior residence effect in convict cichlids (Cichlasoma nigrofasciatum Günther): temporal aspects of establishment and retention, and proximate mechanisms
.
Behaviour
85
,
157
-
182
.
Figler
,
M. H.
,
Cheverton
,
H. M.
and
Blank
,
G. S.
(
1999
).
Shelter competition in juvenile red swamp crayfish (Procambarus clarkii): the influences of sex differences, relative size, and prior residence
.
Aquaculture
178
,
63
-
75
.
Figler
,
M. H.
,
Blank
,
G. S.
and
Peeke
,
H. V. S.
(
2005
).
Shelter competition between resident male red swamp crayfish Procambarus clarkii (Girard) and conspecific intruders varying by sex and reproductive status
.
Mar. Freshw. Behav. Phy.
38
,
237
-
248
.
Fujimoto
,
S.
,
Hirata
,
B.
and
Nagayama
,
T.
(
2011
).
Dominance hierarchy-dependent behavioural plasticity of crayfish avoidance reactions
.
J. Exp. Biol.
214
,
2718
-
2723
.
Gherardi
,
F.
(
2006
).
Fighting behavior in hermit crabs: the combined effect of resource-holding potential and resource value in Pagurus longicarpus
.
Behav. Ecol. Sociobiol.
59
,
500
-
510
.
Han
,
R.
,
Li
,
S.
and
Shi
,
J.-N.
(
2009
).
The territorial prior-residence effect and children's behavior in social dilemmas
.
Environ. Behav.
41
,
644
-
657
.
Herberholz
,
J.
,
McCurdy
,
C.
and
Edwards
,
D. H.
(
2007
).
Direct benefits of social dominance in juvenile crayfish
.
Biol. Bull.
213
,
21
-
27
.
Hsu
,
Y.
,
Earley
,
R. L.
and
Wolf
,
L. L.
(
2006
).
Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes
.
Biol. Rev. Camb. Philos. Soc.
81
,
33
-
74
.
Huntingford
,
F. A.
and
Leaniz
,
C. G.
(
1997
).
Social dominance, prior residence and the acquisition of profitable feeding sites in juvenile Atlantic salmon
.
J. Fish Biol.
51
,
1009
-
1014
.
Hyatt
,
G. W.
and
Salmon
,
M.
(
1978
).
Combat in the Fiddler crabs Uca pugilator and U. pugnax: a quantitative analysis
.
Behaviour
65
,
182
-
211
.
Johnsson
,
J. F.
and
Forser
,
A.
(
2002
).
Residence duration influences the outcome of territorial conflicts in brown trout (Salmo trutta)
.
Behav. Ecol. Sociobiol.
51
,
282
-
286
.
Johnsson
,
J. I.
,
Carlsson
,
M.
and
Sundström
,
L. F.
(
2000
).
Habitat preference increases territorial defence in brown trout (Salmo trutta)
.
Behav. Ecol. Sociobiol.
48
,
373
-
377
.
Karnofsky
,
E. B.
,
Atema
,
J.
and
Elgin
,
R. H.
(
1989
).
Field observations of social behavior, shelter use, and foraging in the lobster, Homarus americanus
.
Biol. Bull.
176
,
239
-
246
.
Kasuya
,
A.
and
Nagayama
,
T.
(
2016
).
Habituation of backward escape swimming in the Marbled crayfish
.
Zool. Sci.
33
,
6
-
12
.
Klar
,
N. M.
and
Crowley
,
P. H.
(
2012
).
Shelter availability, occupancy, and residency in size-asymmetric contests between rusty crayfish, Orconectes rusticus
.
Ethology
118
,
118
-
126
.
Lyko
,
F.
(
2017
).
The marbled crayfish (Decapoda: Camaridae) represents an independent new species
.
Zootara
4364
,
544
-
552
.
Martin
,
P.
,
Kohlmann
,
K.
and
Scholtz
,
G.
(
2007
).
The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring
.
Naturwissenschaften
94
,
843
-
846
.
Momohara
,
Y.
,
Kanai
,
A.
and
Nagayama
,
T.
(
2013
).
Aminergic control of social status in crayfish agonistic encounters
.
PLoS ONE
8
,
e74489
.
Momohara
,
Y.
,
Yoshida
,
M.
and
Nagayama
,
T.
(
2015
).
Serotonergic modulation of social status-dependent behavioural plasticity of the crayfish avoidance reaction
.
J. Comp. Physiol. A
201
,
1063
-
1074
.
Momohara
,
Y.
,
Minami
,
H.
,
Kanai
,
A.
and
Nagayama
,
T.
(
2016
).
Role of cAMP signalling in winner and loser effects in crayfish agonistic encounters
.
Eur. J. Neurosci.
44
,
1886
-
1895
.
Momohara
,
Y.
,
Aonuma
,
H.
and
Nagayama
,
T.
(
2018
).
Tyraminergic modulation of agonistic outcomes in crayfish
.
J. Comp. Physiol. A
204
,
465
-
473
.
Nijman
,
V.
and
Heuts
,
B. A.
(
2000
).
Effect of environmental enrichment upon resource holding power in fish in prior residence situations
.
Behav. Process.
49
,
77
-
83
.
Nijman
,
V.
and
Heuts
,
B. A.
(
2011
).
Aggression and dominance in cichlids in resident-intruder tests: the role of environmental enrichment
.
Neotrop. Ichthyol.
9
,
543
-
545
.
Peeke
,
H. V. S.
,
Sippel
,
J.
and
Figler
,
M. H.
(
1995
).
Prior residence effects in shelter defense in adult signal crayfish (Pacifastacus leniusculus (Dana)): results in same- and mixed-sex dyads
.
Crustaceana
68
,
873
-
881
.
Riechert
,
S. E.
(
1979
).
Games spiders play. III: cues underlying context-associated changes in agonistic behaviour
.
Anim. Behav.
32
,
1
-
15
.
Rillich
,
J.
,
Schlidberger
,
K.
and
Stevenson
,
P. A.
(
2011
).
Octopamine and occupancy: an aminergic mechanism for intruder-resident aggression in crickets
.
Proc. Biol. Sci.
278
,
1873
-
1880
.
Sato
,
D.
and
Nagayama
,
T.
(
2012
).
Development of agonistic encounters in dominance hierarchy formation in juvenile crayfish
.
J. Exp. Biol.
215
,
1210
-
1217
.
Scholtz
,
G.
,
Braband
,
A.
,
Tolley
,
L.
,
Reimann
,
A.
,
Mittmann
,
B.
,
Lukhaup
,
C.
,
Steuerwald
,
F.
and
Vogt
,
G.
(
2003
).
Parthenogenesis in an outsider crayfish
.
Nature
421
,
806
.
Shiratori
,
C.
,
Suzuki
,
N.
,
Momohara
,
Y.
,
Shiraishi
,
K.
,
Aonuma
,
H.
and
Nagayama
,
T.
(
2017
).
Cyclic AMP-regulated opposing and parallel effects of serotonin and dopamine on phototaxis in the Marmorkrebs (marbled crayfish)
.
Eur. J. Neurosci.
46
,
1863
-
1874
.
Snell-Rood
,
E. C.
and
Cristol
,
D. A.
(
2005
).
Prior residence influences contest outcome in flocks of non-breeding birds
.
Ethology
111
,
441
-
454
.
Takahashi
,
K.
and
Nagayama
,
T.
(
2016
).
Shelter preference in the Marmorkrebs (marbled crayfish)
.
Behaviour
153
,
1913
-
1930
.
Tokarz
,
R. R.
(
1985
).
Body size as a factor determining dominance in staged agonistic encounters between male brown anoles (Anolis sagrei)
.
Anim. Behav.
33
,
746
-
753
.
Ueno
,
R.
and
Nagayama
,
T.
(
2012
).
Interlocking of chelae is a key factor for dominance hierarchy formation in crayfish
.
J. Exp. Biol.
215
,
2841
-
2848
.
Vance
,
R. R.
(
1972
).
The role of shell adequacy in behavioral interactions involving hermit crabs
.
Ecology
53
,
1075
-
1083
.
Vogt
,
G.
,
Falckenhayn
,
C.
,
Schrimpf
,
A.
,
Schmid
,
K.
,
Hanna
,
K.
,
Panteleit
,
J.
,
Helm
,
M.
,
Schulz
,
R.
and
Lyko
,
F.
(
2015
).
The marbled crayfish as a paradigm for saltational speciation by autopolyploidy and parthenogenesis in animals
.
Biol. Open
4
,
1583
-
1594
.
Watanabe
,
S.
,
Momohara
,
Y.
,
Minami
,
H.
and
Nagayama
,
T.
(
2016
).
Two types of orienting behaviour during agonistic encounters in the crayfish Procambarus clarkii (Decapoda: Cambaridae)
.
J. Crust. Biol.
36
,
147
-
153
.

Competing interests

The authors declare no competing or financial interests.