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Behavior patterns of individuals in group 1 during hierarchy formation. The frequencies of four different types of behavior (attack, approach, escape and retreat) of individual animals (A-E, labeled from largest to smallest) are plotted over the 20 day period of observation. Each point on day 1 (to the left of the break on the time axis) represents the frequency (occurrences h −1 ) over a 15 min period; points for later days each represent the frequency for a 1 h observation period on that day. Data collection occurred at intervals of between 1 and 3 days (see Materials and methods). In the upper row of plots ('Attack' and 'Approach'), the small divisions above the break along the abscissa represent frequency intervals of 40 h −1 ; in the lower row of plots ('Escape' and 'Retreat'), they represent 20 h −1 .
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The formation of social dominance hierarchies was studied in groups of five juvenile crayfish, 1.3-1.8 cm in length. Animals were grouped together in a small, featureless aquarium after having lived in isolation for more than a month. The occurrence of each of four behavior patterns ('attack', 'approach', 'retreat' and 'escape') was recorded for ea...
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Context 1
... intense throughout the first hour of interaction. One animal in each group quickly emerged as the most active, engaging in more fights and winning more victories than the others. In group 1, animal C, the mid-sized animal in the group, constantly moved from animal to animal, attacking or approaching each, engaging in 250 encounters over the hour (Fig. 1). These attacks were very brief, usually lasting less than 1 s, but were often so vigorous that even the largest animal, A, escaped from C at the first physical ...
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... retreats increased from 50 % to more than 80 % (Fig. 3C). As a result, retreats became the preferred means of withdrawal over escapes by a margin of nearly 4:1 on day 2. Retreats were performed by animals in approximate inverse order of size: E, D and C retreated more frequently than B, and B retreated more frequently than the newly aggressive A (Fig. 1). The preference for retreat over escape persisted during the rest of the period of observation of group ...
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... dependence of different types of behaviors on cardinal dominance Dominant animals in group 1 appear to have gained their position by being aggressive and displaying a higher frequency of attacks and approaches than their opponents (Figs 1, 2). Indeed, in group 1, 95 % of encounters were won by animals that initiated an attack or approach, and in the other groups, the rate of wins followed the same pattern as the rate of attacks (Fig. 2). ...
Citations
... Behavior in crayfsh has been studied in solitary and social settings [1][2][3]. Aggressiveness based on diferences in size, response to missing cheliped, and diferential exposure to pharmacological or hormonal agents has been studied in pairs of crayfsh (dyads) and in groups [4,5]. Te extremely aggressive behaviors seen in an intense battle, such as removing the opponent's limbs or fipping them over to cut the articulation membrane in the abdomen, were ranked as the most aggressive score as this would infict a life-threatening wound [6]. ...
... Te extremely aggressive behaviors seen in an intense battle, such as removing the opponent's limbs or fipping them over to cut the articulation membrane in the abdomen, were ranked as the most aggressive score as this would infict a life-threatening wound [6]. More recently, stability of the social hierarchy over time has also been assessed using behavioral indices [3,7]. Furthermore, Gherardi and Pieraccini [8] developed detailed indices for 20 diferent behavioral patterns for quantifying agonistic encounters in crayfsh. ...
Animal behavior is a useful way to evaluate the environment and can be a predictive tool to assess not only the effects of treatments in a laboratory setting, but also the status of ecological habitats. As invasive species of crayfish encroach on territories of native species, the social behaviors and interactions can be informative for ecological studies. For a wider and more impactful effect, training community scientists using a scoring system to record the social interactions of crayfish that includes both the level of aggression and intensity would provide useable data to monitor the environment. Amateur scientists with little training were fairly reliable in their average scoring of the crayfish and the maximum behavior score with an expert as well as among themselves. However, the number of interactions was not as a reliable metric to compare with the expert or just among the amateurs.
... These data might suggest a self-assessment strategy at Specifically, as sex-based size difference skewed positive (i.e., towards larger males than females), the likelihood of male winner increased but the exact point these lines crossed the 0.5 outcome (horizontal dashed line) was dependent upon the lesion treatment. Vertical black lines at x = -10 and x = 10 denote the "size matched" area of the graph (see Pavey & Fielder, 1996;Issa et al., 1999;. first glance; however, neither loser nor smaller contestant size regressed significantly with contest duration (Table 4) which is expected in a self-assessment type strategy (Table 3; Taylor & Elwood, 2003;Arnott & Elwood, 2009). ...
... Solid black lines at x = -10 and x = 10 denote the "size matched" area of the graph. Within an approximately 10% size difference, crayfish are considered the same size (see Pavey & Fielder, 1996;Issa et al., 1999;. Positive sex-based size difference numbers denote larger males while negative sex-based size difference numbers denote larger females. ...
... Positive sex-based size difference numbers denote larger males while negative sex-based size difference numbers denote larger females. Solid black lines at x = -10 and x = 10 denote the "size matched" area of the graph (see Pavey & Fielder, 1996;Issa et al., 1999;. Symbols with solid black squares and a solid black line indicate fights under the non-lesion treatment and the best fit exponential decay line, respectively; symbols with open circles and a red solid line indicate fights under the female lesion treatment and the best fit exponential decay line. ...
Male and female differences in contest strategies present a valuable exploration of varied access to relevant ecological information. Crayfish studies have revealed that males and females likely use different sources of information to dictate contest persistence and the difference becomes most apparent in mixed-sex contests. We examined the role of chemical information in mixed-sex contest dynamics and assessment by randomly pairing mixed-sex pairs that were either size-matched or size asymmetric. The lesion treatments consisted of eliminating olfactory cells on the antennules, the main organ for chemical detection in crayfishes. Dyads were classified as control (both intact), female-lesioned (females lesioned, males intact), or male-lesioned (females intact, males lesioned). Statistical analysis revealed that sex-based size difference, lesion treatment, and winner’s sex dictated contest duration. Regressions did not reveal evidence of one particular assessment strategy for control dyads, but male- and female-lesioned contests demonstrated weak relationships indicative of a possible self-assessment strategy. Behavioral network analyses indicated that chemical information is important for transitions between behavioral states and that the sexes use this information differentially. We suggest chemical information is important for both males and females in contest assessment, but the information contained in the signal or how the participants use the information for assessment likely differs across the sexes.
... The presence of other crayfishes causes stress and greater energy losses (Karaban and Stęplowski 2018). Males are submissive and prone to courtship towards females, while males are extremely aggressive towards males (Issa et al. 1999). Global warming may conducive to the expansion of the red swamp crayfish population, which in interaction with high ecological plasticity may enable the expansion of this species (Hellmann et al. 2008;Frelich and Reich 2009; Lee and Park 2019). ...
Invasive alien species are one of the major problems in Polish fauna and flora. They can displace native species and cause economic losses. Such animals as red swamp crayfish have a wide tolerance to changing living conditions, which means that their range of occurrence increases over time. The current area of red swamp crayfish in Poland includes several locations, but reports indicate that this species inhabits many other reservoirs. It is very important that the red swamp crayfish population is regularly monitored, which may limit the number of this crustacean in Polish waters.
... While food availability is unlikely to be a limiting factor in nature because crayfish are omnivores (Holdich 2002), it was used as a proxy for density-dependent effects. Juvenile crayfish form social dominance hierarchies (Issa et al. 1999;Sato and Nagayama 2012) and dominant individuals have increased access to food (Herberholz et al. 2007). Increasing population density is thus expected to limit resource availability, increase competition intensity (Capelli and Hamilton 1984), and induce stress. ...
Invasive alien crayfish threaten the diversity of freshwater ecosystems and native crayfish fauna. In Europe, this is largely due to transmission of the crayfish plague to susceptible native crayfish. Many invasive species tolerate crayfish plague, but the infection still has the potential to reduce the fitness of a tolerant host due to energy trade-offs between immune response maintenance and life-history traits, such as growth and reproduction. In combination with other unfavourable conditions, such a response could alter further invasion success of an otherwise successful crayfish invader. We examined whether repeated infection with one of the most virulent haplogroups of crayfish plague agent ( Aphanomyces astaci ) affects growth or survival of the juvenile marbled crayfish ( Procambarus virginalis ). Juveniles were exposed to i) two levels of pathogen concentrations, and ii) two different feeding regimes under the higher pathogen concentration. In all performed trials, repeated infection reduced growth rates, while the combination of recurring infection and food limitation significantly increased mortality. The average energy cost of the immune response was estimated at 12.07 J/day for individuals weighing 0.3 grams. Since infections were frequent and pathogen concentrations high, results suggest that marbled crayfish is resistant to A. astaci pathogen and its survival is only affected by adding the stress of food limitation. The survival of almost half of the individuals exposed to high pathogen loads and extreme food limitation indicates that chronic infection by crayfish plague is unlikely to be an important factor impeding invasion success of the marbled crayfish, even under harsh conditions. Our results add to the growing body of evidence that marbled crayfish has potential to become one of the most successful freshwater invaders.
... The brilliant work of Huxley at the end of the 19th century already described many crayfish behaviors, their natural history and basic physiology, and provided guidance and concepts for future researchers (Huxley, 1880). Today, ethograms of many crayfish escape Herberholz and Marquart, 2012) and social behaviors (Heckenlively, 1970;Copp, 1986;Figler et al., 1995;Yeh et al., 1997;Issa et al., 1999;Vorburger and Ribi, 1999;Herberholz et al., 2001;Baird et al., 2006) have been developed and the underlying circuits are known to varying degrees. This has already established them as model organisms for social dominance (Edwards et al., 2003;Abe and Nagayama, 2021), anxiety (Fossat et al., 2014), intoxication (Swierzbinski et al., 2017;Venuti et al., 2021), and decision making (Herberholz and Marquart, 2012). ...
For over a century the nervous system of decapod crustaceans has been a workhorse for the neurobiology community. Many fundamental discoveries including the identification of electrical and inhibitory synapses, lateral and pre-synaptic inhibition, and the Na+/K+-pump were made using lobsters, crabs, or crayfish. Key among many advantages of crustaceans for neurobiological research is the unique access to large, accessible, and identifiable neurons, and the many distinct and complex behaviors that can be observed in lab settings. Despite these advantages, recent decades have seen work on crustaceans hindered by the lack of molecular and genetic tools required for unveiling the cellular processes contributing to neurophysiology and behavior. In this perspective paper, we argue that the recently sequenced marbled crayfish, Procambarus virginalis, is suited to become a genetic model system for crustacean neuroscience. P. virginalis are parthenogenetic and produce genetically identical offspring, suggesting that germline transformation creates transgenic animal strains that are easy to maintain across generations. Like other decapod crustaceans, marbled crayfish possess large neurons in well-studied circuits such as the giant tail flip neurons and central pattern generating neurons in the stomatogastric ganglion. We provide initial data demonstrating that marbled crayfish neurons are accessible through standard physiological and molecular techniques, including single-cell electrophysiology, gene expression measurements, and RNA-interference. We discuss progress in CRISPR-mediated manipulations of the germline to knock-out target genes using the ‘Receptor-mediated ovary transduction of cargo’ (ReMOT) method. Finally, we consider the impact these approaches will have for neurophysiology research in decapod crustaceans and more broadly across invertebrates.
... Empirically, many studies have found that winners of cannibalistic interactions are larger than losers (Claessen et al. 2004;Ibáñez and Keyl 2010;Barkae et al. 2014;Rojas 2014), although exceptions exist when larger individuals are weakened (Richardson et al. 2010) or when individuals compensate for their size with increased aggressiveness (Issa et al. 1999). Kinship between individuals can also explain aggression. ...
In juveniles extreme intraspecies aggression can seem counter-intuitive, as it might endanger their developmental goal of surviving until reproductive stage. Ultimately, aggression can be vital for survival, although the factors (e.g., genetic or environmental) leading to the expression and intensity of this behavior vary across taxa. Attacking (and sometimes killing) related individuals may reduce inclusive fitness; as a solution to this problem, some species exhibit kin discrimination and preferentially attack unrelated individuals. Here, we used both experimental and modeling approaches to consider how physical traits (e.g., size in relation to opponent) and genetic relatedness mediate aggression in dyads of cannibalistic Dendrobates tinctorius tadpoles. We paired full-sibling, half-sibling, and non-sibling tadpoles of different sizes together in an arena and recorded their aggression and activity. We found that the interaction between relative size and relatedness predicts aggressive behavior: large individuals in non-sibling dyads are significantly more aggressive than large individuals in sibling dyads. Unexpectedly, although siblings tended to attack less overall, in size-mismatched pairs they attacked faster than in non-sibling treatments. Using a theoretical model to complement these empirical findings, we propose that larval aggression reflects a balance between relatedness and size where individuals trade-off their own fitness with that of their relatives. Lay Summary Before you eat someone, you have to attack them first. Here, we investigated the factors that shape aggression in the cannibalistic tadpoles of the dyeing poison frog. We find that aggression depends on both size and relatedness: when set in pairs, large tadpoles are half as aggressive towards their smaller siblings than to nonsibs. It looks like belonging to the same family provides some protection against aggression, though no one is ever truly safe.
... When a new social group is formed, individuals may use a variety of strategies to establish dominance ranks, including sensory cues (e.g., auditory, olfactory, or visual), in addition to aggression. When utilizing aggression, "a pecking order" can often be established relatively quickly, even within minutes (Issa et al., 1999;Meese & Ewbank, 1973;. The presence of a social hierarchy is beneficial to prevent prolonged and intense fighting, as the establishment of a social relationship can govern future interactions, including approach and retreat behaviors (Casey et al., 2015). ...
Social instability (SI) occurs when there is competition over social status. Reduced certainty of social status can lead to heightened aggression, which can increase physiological stress responses as individuals prepare to fight for their social status. However, adults can use proactive coping mechanisms to reduce the physiological stress induced by SI, such as increasing affiliation. Very little is known, however, about the behavioral and hormonal effects of SI early in development. Filling these gaps in knowledge would add to the fields of primatology and developmental and comparative psychology. We
conducted an opportunistic study of a peer group of 18 rhesus macaque (Macaca mulatta) yearlings before and during SI. We used social network analysis to measure individuals’ dominance certainty
(DC; in their aggressive and submissive network) and their position in affiliative networks (grooming and play) and analyzed hair cortisol concentrations (HCCs). As predicted, during SI, we observed a
decrease in DC, indicating that individuals had less stable dominance positions. As well, during SI, we observed increased rates of social grooming and decreased rates of social play, reflecting potential coping mechanisms. More socially connected individuals in social grooming and social play networks received higher levels of coalitionary support. Contrary to predictions, DC did not predict HCCs; rather, individuals that were more connected in the social play network exhibited smaller increases in HCCs during SI, revealing a potential buffering effect of social play. Our results underscore the need for further research on the effects of SI during ontogeny.
... Additionally, this pattern was not observed in 5.1-cm traps, so we are unable to explain this observation. Furthermore, some research indicates that larger crayfish intruders maintain dominance at shelter resources , Issa et al. 1999). However, our study only recorded data on which crayfish occupied ARTs and not the exchange of dominance between previous and current burrow occupiers. ...
Invasive species are a widespread threat to stream ecosystems across the planet. In Southern California,USA, the invasive red swamp crayfish Procambarus clarkii (Girard, 1852) poses a significant threat to native aquatic fauna. Studies have suggested that artificial refuge traps (ARTs) resembling crayfish burrows can be used to remove invasive crayfish, but, to date, no studies have focused on optimizing ART design and deployment to maximize crayfish catch. This month-long study tested the effect of modifications on ART diameter, color, and soak time on P.clarkii catch effectiveness across 160 traps. We evaluated catch data by creating multiple candidate generalized linear mixed models predicting P. clarkii catches with different modeling parameterizations and a priori hypothesized predictor variables. During the study period, ARTs removed a total of 240 red swamp crayfish with no incidental bycatch. Larger P. clarkii(2–6-cm carapace length) were found more frequently in 5.1-cm-diameter traps, andsmallerP. clarkii(1–4 cm) were found more frequently in 2.5-cm-diameter traps. Catch numbers varied between trap types, with black-colored 5.1-cm-diameter traps removing the greatest amount of the totalP. clarkii caught in the study (mean=50.27, SD=50.29; 35% of the total caught) and black-colored 2.5-cm-diameter traps removing the least amount (mean=50.09, SD=50.55; 12% of the total). Further, ART deployment duration was an important predictor variable for candidate models, where ARTs with 4-d and 7-d deployment durations had lower catch/unit effort than traps with 1-d and 2-d deployments. This factorial experiment is the 1st study to suggest specific design modifications to ARTs that optimize invasive red swamp crayfish removal without incurring non-target incidental bycatch. This study demonstrates that ARTs can be a valuable tool for conservation managers interested in restoring streams through invasive crayfish removal, especially where there are sensitive biological resources.
... Virile crayfish are similar in size to rusty crayfish, and crayfish size is known to be a determinant of competitive outcomes among individuals and species (Pavey and Fielder, 1996;Issa et al., 1999). Although this species has most commonly been found in rocky habitat around the Great Lakes, in this study virile crayfish were often in harbors with primarily sandy habitat or in mucky habitat with turbid water and a high density of macrophytes. ...
Crayfish represent important links in aquatic food webs because they have diverse, omnivorous diets and are an important source of energy for fishes and birds. Crayfish have the ability to increase sediment transport through bioturbation, some are considered ecosystem engineers due to their burrowing habits, and crayfish invasions have been linked to large declines in biodiversity and changes in ecosystem structure and function. Despite their ecological importance and the threats that invasive crayfishes pose, the distribution of crayfishes in the Laurentian Great Lakes is not well studied. Here, we report on four years of intensive crayfish surveys in the southwestern portion of the Lake Michigan Basin, a region with diverse freshwater ecosystems and few previous records of crayfish distribution. From 2015 to 2018, baited minnow traps and SCUBA were used to document the distribution and abundance of crayfish across streams, rivers, inland lakes, and Lake Michigan. Six species of crayfish were captured, including two invasive species. The invaders are the widely distributed and abundant Faxonius rusticus (rusty crayfish) and Procambarus clarkii (red Swamp crayfish), a species early in the invasion phase. Native species were found in fewer habitat types and were less abundant than invasive F. rusticus. Comparing our results to previous sampling showed that native crayfish distribution and diversity have declined at the same time that F. rusticus has spread over recent decades. There is potential for new and recently introduced invaders, such as the red swamp crayfish, to further alter ecosystems.
... Crayfish is a good model organism to investigate the interaction between agonistic and mating behaviours. Agonistic encounters and formation of dominant and subordinate relationships are well characterized both physiologically and behaviourally (Bovbjerg, 1953(Bovbjerg, , 1956Lowe, 1956;Huber et al., 1997;Huber & Delago, 1998;Issa et al., 1999;Goessmann et al., 2000;Herberholz et al., 2001Herberholz et al., , 2007Daws et al., 2002;Bergman et al., 2003;Zulandt et al., 2008;Graham & Herberholz, 2009;Sato & Nagayama, 2012;Momohara et al., 2013Momohara et al., , 2015Momohara et al., , 2016Momohara et al., , 2018Watanabe et al., 2016). Mating processes are also known in detail (Berrill & Arsenault, 1984;Stebbing et al., 2003;Gherardi et al., 2006;Aquiloni & Gherardi, 2008a,b;Horner et al., 2008). ...
Intraspecific communication is essential for agonistic and mating behaviours. Agonistic strategy of males must change according to the sex of opponents and that of females is also dependent on their physiological state as to whether they are brooding or not. We have analysed here the agonistic encounters between pairs of male and female crayfish in various combinations to reveal the interaction between agonistic and mating behaviours. After male crayfish became dominant, they aggressively chased subordinate males with attacks, while they did not attack female opponents. Furthermore, the agonistic behaviour of males changed depending on whether females were ovigerous or not. On the other hand, two females showed intense combats despite being ovigerous or not. Crayfish discriminated the sex of opponents via chemical signals in the urine. However, the dominant and subordinate social order of crayfish had no effect on selecting mating partners.
