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Sensory Systems and Environmental Change on Behavior during Social Interactions

Sensory Systems and Environmental Change on Behavior during Social Interactions Hindawi Publishing Corporation International Journal of Zoology Volume 2013, Article ID 573802, 16 pages http://dx.doi.org/10.1155/2013/573802 Research Article Sensory Systems and Environmental Change on Behavior during Social Interactions 1 2 1 S. M. Bierbower, J. Nadolski, and R. L. Cooper Department of Biology & Center for Muscle Biology, University of Kentucky, Lexington, KY 40506-0225, USA Department of Mathematical and Computational Sciences, Benedictine University, Lisle, IL 60532, USA Correspondence should be addressed to R. L. Cooper; rlcoop1@email.uky.edu Received 21 December 2012; Revised 13 March 2013; Accepted 15 March 2013 Academic Editor: Randy J. Nelson Copyright © 2013 S. M. Bierbower et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. eTh impact of environmental conditions for transmitting sensory cues and the ability of craysfi h to utilize olfaction and vision were examined in regards to social interactive behavior. eTh duration and intensity of interactions were examined for conspecific crayfish with different sensory abilities. Normally, vision and chemosensory have roles in agonistic communication of Procambarus clarkii; however, for the blind cave crayfish ( Orconectes australis packardi), that lack visual capabilities, olfaction is assumed to be the primary sensory modality. To test this, we paired conspecifics in water and out of water in the presence and absence of white light to examine interactive behaviors when these various sensory modalities are altered. For sighted crayfish, in white light, interactions occurred and escalated; however, when the water was removed, interactions and aggressiveness decreased, but, there was an increase in visual displays out of the water. The loss of olfaction abilities for blind cave and sighted crayfish produced fewer social interactions. The importance of environmental conditions is illustrated for social interactions among sighted and blind crayfish. Importantly, this study shows the relevance in the ecological arena in nature for species survival and how environmental changes disrupt innate behaviors. 1. Introduction established Barnard and Sibly [13] producer-scrounger game in which mixes of strategies work better than all one or Social relationships may take many forms when organisms the other of a specific strategy. er Th e are obvious ecological live in a group, and oen ft times, the individuals must benefits for being the dominant individual and little point in determine their status within a social structure [1–3]. Social interacting if there is an absence of benefits with aggressive dominance is a form of a social relationship in which interactions. us, Th the benefit of interactions must account individuals aggressively interact repeatedly. The interaction not only for the resource, but also the cost in obtaining between individuals is a well-studied sequential series of the resource. The dominate individuals oeft n have increased interactions, with each individual having the option of access to resources such as mates, food, and shelters [14, terminating or continuing the interaction/contest at any time. 15]. However, this may not always be the case since many The consequence of these interactions most likely results other factors play a role such as the value of the resource in a dominant individual who repeatedly wins encounters [16], the inability to monopolize a resource [17], and the against a subordinate [3]. eTh refore, agonistic encounters will loss of resources’ due to stealing of stores/caches by other generally establish social hierarchies between individuals in individuals [18]. Furthermore, females with young often rise apopulation[4–9]. Dominance hierarchies are known to in the social ranks to better provide for their young [19], as decrease aggressive interactions between individuals based well as hungry subordinate individuals oen ft win encounters upon social status, therefore stabilizing the population over against dominants for access to food [20, 21]. time [10, 11]. eTh re are many factors involved in the establishment of Smith [12]suggeststhatrankmay be astrategyindi- social dominance, and it is well documented that environ- viduals adopt to maximize tfi ness in the population based mental cues play a major role in the outcome of social interac- upon theroleofother individuals. Thiscorrelateswiththe tions whether through chemosensory (odors, [22, 23]), visual 2 International Journal of Zoology (opponent posturing, [24, 25]), and/or tactile cues (physical examine whether behavioral, morphological, and/or physio- combat, [4, 5, 7, 8]). logical evolutionary adaptations may have evolved uniquely An ideal model system to study social interactions is with to their species based upon the cave environment. Since crayfish since typical interactions have been well documented cave crayfish have a reduced optic system and have more for decades. Crayfish are known to form social hierarchies olfactory projection neurons than surface sighted crayfish, aer ft very aggressive interactions [ 4–9, 26, 27]. Typically, the it was suggested they have more neural processing related encounters escalate from visual threats of defense postur- to olfaction [39]. Cave craysfi happeartorelyprimarily on ing to actual physical confrontations that include cheliped olfactory and tactile modalities, while surface craysfi h rely grasping andmoreaggressivebehaviors whereone will try primarily on visual and olfactory to assess and monitor to dismember or even kill another individual. their surroundings. Since these cave crayfish do have caudal Currently, most studies observing social interactions photoreceptors in their 6th abdominal ganglion and respond occurinanaturalfieldsiteoralocation that mimics the to white light, studies were performed in white and red typical environment. While this gives insights into typical lights. eTh caudal photoreceptors are not sensitive to the behaviors, little is known of the interaction dynamics when red light used, as assayed in behavioral studies [40]. In naturalchanges occursuchaswhenanorganismleavesthe accordance with the above information, it is logical that cave aquatic environment or when sensory systems are dimin- craysfi h do not show the typical postural behaviors (visual ished. Crayfish leave the water for various reasons such as to display) identified in social encounters within their natural find food, mates, or when excessive competition may drive cave environment. We hypothesized that such displays would them to look for other niches. eTh environmental change not be beneficial since conspecifics are not able to observe with the absence of water would eliminate the typical escape the visual display. While studies have addressed the neural response (i.e., tail flip) which allows for a fast retreat from structure of the optic systems [39]and theeeff ctsoflight on conspecifics. In addition, the absence of water results in other social interactions [40], the typical behaviors of cave crayfish factors influencing social interactions, such as a higher energy have not been as thoroughly studied as with surface crayfish. demand for movement mainly due to the lack of buoyancy, Currently, little is known of interaction dynamics in the a greater probability of injury due to a slower response in absence of water which eliminates the typical escape response movement, as well as retreat and also the lack of assessment (i.e., tail flip) and/or with diminished chemosensory systems through chemical cues of not only conspecifics, but also the in either species of crayfish. environment in general. us, Th an organism is at greater risk Chemical signals are also important sources of informa- since they lack the ability to assess their opponent and/or tion in aquatic environments where visibility maybe limited locate asafeplace forretreat.This is especially true fora when compared to terrestrial open environments [40]. Cray- species evolutionarily lacking a sensory modality. Hence, fish are known to have a [ 41, 42] well-developed olfactory it is of interest to examine the eeff ct of diminished visual system, and studies have shown that chemical signals play and olfactory/chemosensory sensory system. This is possible an important role in many aspects of their life [23, 43, 44]. through studies in the absence of white light and the removal Specifically in agonistic encounters, chemical signals appear of the primary chemosensory appendage (i.e., antennules) in to be more important than other oen ff sive displays and surface species, as well as studies in an evolutionarily distinct signals for settling a gfi ht [ 45]. Interestingly, research has species of crayfish which lack the visual sensory modality. shownthatsomespecies areabletorecognize individuals Although vision and tactile have been suggested to be that they have encountered in the recent past such as two very important in social interactions for mediating the species of hermit crabs [46–48], crab [49], mantis shrimp transfer of information, the full understanding on the ways Gonodactylus festae [50, 51], lobsters Homarus americanus these two sensory cues are used in agonistic communication [52], and crayfish [ 53]. It has been shown that the individual remains unclear. It has been well studied and shown that recognition is based upon chemical signals that are emitted vision is important for agonistic communication in other during social interactions [54–56] in crustaceans [57]. The decapod species, such as dd fi ler crabs [ 28–30], hermit crabs chemical signals are important in maintaining the stable [31–35], lobsters [36], and mantis shrimp [37]. Due to this dominance hierarchies. obvious factor in so many other decapod crustaceans, we Chemical cues are known to be involved in the establish- assume that the visual sensory cue would also be very ment of social hierarchies and are known to impact behavior important for information exchange among crayfish. We [58, 59]. Bovbjerg [5] rfi st suggested that both vision and chose to separate the roles of vision and chemosensory in tactile are involved in the establishment of social hierarchies, the agonistic communication of P. clarkii by conducting and he also demonstrated that antennae are important for experiments in red light (not visible to P. clarkii)aswellas tactile orientation. eTh antennule is considered the organ removing the antennules, both independently and additively most specialized for chemosensory detection and plays a to a red light environment. eTh study of vision in this species leading role in tracking odor plumes [60]and individual is particularly appropriate, given that P. clarkii are normally recognition [61]. One way to address the influence of sensory active under a wide range of environmental light levels, and cues is to remove important sensory systems individually and we mimic periods of dusk and dawn which are known to be simultaneously. Specifically, by removing the antennules and particularly active time points [38]. Blind cave crayfish ( Orconectes australis packardi) lack vision through the absence of white light (provide red light), one can understand the reliance on sensory cues. visual capabilities; therefore, they provide the opportunity to International Journal of Zoology 3 It is apparent that many environmental cues determine the outcome of social interactions. With the assumption that all group members begin with equal gfi hting abilities, environmental eeff cts or diminished sensory cues will most likely disrupt the typical intrinsic behavior. Furthermore, when multiple cues are diminished, the inu fl ence may be additive or behave synergistically in altering a behavior. u Th s, by examining reliance on single sensory systems on well-defined social behavior, we can begin to understand Figure 1: Blind cave crayfish, Orconectes packardi australis,engaged environmental impacts on populations/species. We com- in an agonistic encounter. pared social interactions in white light to experiments in red light to understand the photoreceptors influence on social interactions. 2. Methods Past studies have examined many extrinsic factors that influence intraspecific aggression, such as shelter acquisition 2.1. Animals. Crayfish, Procambarus clarkii (sighted), mea- [19, 62, 63], chemical communication [5, 23, 64], mating suring 5.0–6.25 cm in body length were obtained commer- [65], food preferences [66], and starvation [67, 68]. An area cially (Atchafalaya Biological Supply Co., Raceland, LA, not yet addressed is the extrinsic factor of “out of water” USA). Crayfish, Orconectes australis packardi (Rhoades) (the for crayfish social interactions, and it is unclear whether the blind crayfish), measuring 4.6–6.4 cm, were obtained from hydrodynamics of natural habitats allow for the successful the Sloan’s Valley Cave System near Somerset, KY, USA (state useofchemicalsignals andtypical behavior during social collecting permits were obtained for this study; Figure 1). A interactions in nature. us, Th the purpose of this study is to totalof25sighted and15blind craysfi hwereusedinthe present quantitative analysis of environmental influence on study. Craysfi h pairs were randomly chosen from the na ¨ıve social interactions in two species of crayfish with special population stock. eTh order in which the trials occurred reference to reliance of dieff rent primary sensory modali- was random. No two crayfish were paired together more ties. than once; thus, all encounters were with conspecifics not Intrinsic and extrinsic factors aeff ct intraspecific aggres- previously known to each other. Only male crayfish were sion in many ways, and both should be examined for the used in this study. Animals were housed individually in impact on agonistic behavior. Herein, a simple additive rectangular plastic containers and cared for in the same model for this integration of multiple sensory systems as manner, except for O. a. packardi that were covered with black well as multiple environmental factors in an individual’s plastic to omit light in an aquatic facility within our regulated- expected gfi hting ability determined the impact of additive temperature laboratory (17–20 C). P. clarkii were on a 12- effects. Examination of environmental influence on behavior hour period light-dark cycle. All crayfish were fed dried was through the measure of fighting strategy and intensity fish pellets weekly before and throughout the experiments. of interaction in two species (Procambarus clarkii, sighted Craysfi hhandlingwas conductedbyusing aglass beaker surface crayfish and Orconectes australis packardi, blind cave to transfer crayfish from one container to the another. Due crayfish). to housed containers being cleaned weekly, craysh fi were Due to distinct behavioral, anatomical, biochemical, mor- handled oeft n; the limited handling during experimentation phological, and/or physiological adaptations of cave organ- is assumedtohavelittletonoeeff ct on theinternalstatusof isms, there is a fascination and interest in understanding how the crayfish. Only crayfish in their intermolt stage, possessing they are able to adapt and survive in extreme environments. all walking legs and both chelipeds were used in these studies. Cave crayfish show the general characteristics of anatomical and morphological adaptations of most cave organisms. Specifically when compared to surface crayfish, cave crayfish 2.2. Social Interactions. Initial experiments (i.e., low light) are smaller in size, have longer/thinner appendages, possess were focused on characterizing the general behavioral inter- highly developed nonvisual sensory capabilities, and lack actions for both species of crayfish. Crayfish were randomly pigment and eyes [69]. In addition, behavioral, physio- distributed into fourteen different conditions as discussed logical, and biochemical adaptations have been identified below. Social interactions were staged in size-matched males. in cave crayfish such as a decrease in locomotion and An interaction behavioral scoring index was developed oxygen consumption, as well as a decrease in metabolic (Table 1(a)) for species comparison of P. clarkii and O. rates [70]. eTh se are related to a reduction in energy from australis packardi. Observational preexperimental trials iden- limited food sources and/or oxygen availability in cave tified typical crayfish behavior to establish a quantifiable systems [71–73]. u Th s, these distinct evolutionary adapta- scale for interactions based on both aggressiveness, as well tions allows for studies discerning behavioral differences as intensity (time duration of the interaction, Table 1(b)). in two species of crayfish. Another goal of this study was Craysfi h male pairs of approximate equal size were staged in to identify species-specific behaviors through comparison a glass aquarium and videotaped for one hour, allowing for of cave and a surface species, as well as determining the interaction without outside interference. The crayfish were environmental and olfactory influence on intrinsic behav- monitored indirectly with a TV monitor. Trials conducted iors. in low light in the water served as controls for the sighted 4 International Journal of Zoology Table 1: Social interaction scoring bioindex. (a) Indicates the Most of the general characteristics are previously de- behavioral scoring bioindex used to quantify behavior during each scribedinDingleand Caldwell [74]. Interactions typically trial in the experimental conditions. (b) Indicates the intensity scale began with an invasion of territory or an acknowledgment/ based upon time duration in which the pairs were engaged in a stando.ff Termination of the interaction occurred when the specific behavior. observer determines that individuals no longer appear to be directing behavior at each other. Communication may (a) be occurring,but sincethe purposeofthisstudy was 0 No interaction to concentrate on aggressive interactions, no attempt was 1. Territory invasion made to analyze other possible communicative behaviors. 2. Intentional touching Quantification of behavior was based upon total number of interactions as well as the length of each individual 3. Acknowledgment interaction. 4. Threat display Each trial was critically analyzed to categorize craysfi h 5. Chase behavior, as well as identify general behavioral trends within 6. Grasp/strike and across species. For each environmental condition (i.e., 7. Dismemberment lowlight,red light, andnoantennules),five trials (𝑁 = (b) 5) were runinthe waterand vfi etrials (𝑁 = 5) were run out of the water. All trials were digitally recorded and 0.1 1–15 seconds analyzed through video analysis to record behavioral scores 0.2 16–30 seconds and intensity. To understand behavioral trends, 3D graphs 0.3 31–45 seconds combined all trials together for comparison of the type of 0.4 >45 seconds behavior as well and intensity of each encounter. eTh duration of an interaction was used as a measure of interaction intensity. Since interactions are known to be relatively short, crayfish, while trials conducted in red light in water act atimescale wasused(Table 1(b)). as controls for blind crayfish. The index was then used to quantify each of the trials across conditions and species comparison. Behavioral scores were assigned to pairs of 2.4. Environmental Conditions. The various environmental crayfish (not individual scoring) for every interaction that conditions that were used are listed in Table 2. Social interac- occurred during the 60-minute time period. tions were examined in and out of water in low light (25 lux). “In water” studies used a glass aquarium (20 cm× 10 cm× 2.3. Behavioral Analysis. Previous research and prior obser- 12 cm) 4 cm filled from the top with aerated water. “Out of vation of aggressive interactions between individuals indicate water” studies were conducted using the same aquarium but that the behavior could be classiefi d into several rather dis- without water and still providing wet sand for the animals tinct categories. These categories represent behavior patterns to walk on. “In water” studies (control) for both sighted in what are relatively stereotyped and which are known to and blind crayfish were compared to other environmental be typical behaviors of sighted craysh fi . Brieyfl the behavioral conditions to determine changes in intrinsic behaviors. This acts established are as follows (also see Table 1(a)). part of the study examined: (1) sighted “in water,” (2) sighted “out of water,” (3) blind “in water,” and (4) blind “out of water”. 0-No interaction: no encounter without any evidence Social interactions were also observed in red light. Red of awareness of other individual. lightconditionsusedafilteredred light(2.5Lux)toremove 1-Territory invasion/approach/retreat:deliberate the visual sensory stimulation for the sighted crayfish and the movement towards other individual and a direct, stimulation of the caudal photoreceptors in the cave crayfish. initiation into conspecifics space and/or movement The red light (Kodak Adjustable Safeway Lamp, 15 watts), away. was previously noted to be a wavelength not detected by crayfish [ 9, 40] thus providing no visual sensory stimulation. 2-Intentional touching: a short rapid movement for- The purpose is to examine the reliance of visual cues for ward directed at individual. sighted crayfish out of water when chemosensory cues are 3-Acknowledgment/standoff :facingoneanotherwith- diminished. Furthermore, using blind crayfish in red light out visual threat display. allowed us to help determine if low light induces a stress 4-Meral spread/threat display: outward raising and response that influences social behavior. We examined these spreading of the chelipeds. conditions in this part of the study: (1) sighted/in water/red light, (2) sighted/out of water/red light, (3) blind/in water/red 5-Chase:pursuit aeft r theindividual. light, and (4) blind/out of water/red light (Table 2). 6-Grasp/strike: a blow to or seizing of other individ- The removal of olfactory cues was conducted by removing ual. the antennules (primarily sensory system for chemical detec- 7-Dismemberment:veryaggressiveactiontoindivid- tion) with sharp scissors at the base of the antennules by the ual in which dismemberment or likelihood of killing first annuli. er Th e was no death associated with antennulec- is apparent. tomy as this is not that invasive of a surgery for crayfish. In International Journal of Zoology 5 Table 2: Social interaction conditions for both species of crayfish. Social interactions were observed both in and out of the water for sighted and blind crayfish. Assessment of different sensory modalities impact on intrinsic behavior was examined through methodical removal of one or many sensory cues. Sighted Blind In water Out of water In water Out of water Low light Low light Low light Low light Red light Red light Red light Red light Low light/no Low light/no —— antennules antennules Red light/no Red light/no Red light/no Red light/no Figure 2: Schematic representation for the placement of the record- ing wires for monitoring the heart from a crayfish (Procambarus antennules antennules antennules antennules clarkii.). On the dorsal carapace, large arrows represent the two wires which spanned the rostral-caudal axis of the heart to monitor any change in the dynamic resistance, which is used as a measure of heart fact, there is little blood loss as well since this is not that wide rate. of a region as compared to the very base of the antennules next to the cephalothorax. eTh animals were held for 3 days for recovery aeft r antennulectomy. “In water” and “out of stainless steel wires and recorded on-line to a PowerLab via water” studies were again conducted for both species of cray- a PowerLab/4SP interface (AD Instruments). All events were fish. The purpose of removing the antennules was to further measured andcalibratedwiththe PowerLab Chartsoftware understand the reliance of visual cues for sighted crayfish and version 5.5.6 (AD Instruments, Australia). Previous studies to understand impacts on social behavior for blind craysfi h if showed that 3 days was enough time for the animals to there was a lack of environmental olfactory cues. These set return to physiological measurements similar to levels prior of conditions compared (1) sighted/in water/no antennules, to handling [78]. Cave crayfish typically have a thinner, more (2) sighted/out of water/no antennules, (3) blind/in water/no brittle exoskeleton resulting in more delicate handling during antennules, and (4) blind/out of water/no antennules. wiring. To determine the reliance on environmental cues during Analysis of the response consisted of heart rate in social interactions for sighted crayfish, both chemosensory beats per minute (BPM). HR was monitored in and out of and visual cues were removed. Social interactions were water under control conditions to determine physiological examined for sighted crayfish only in red light and with responses during social interactions. This provided an inter- the removal of antennules in order to compare these two nal measure to external cues. The experimental procedure conditions: (1) sighted/in water/red light/no antennules and consisted HR recordings before, during, and after social (2) sighted/out of water/red light/no antennules. interactions. HR was analyzed to provide a BPM to note changesinthe internal response baseduponinteractions, as 2.5. Recording ECGs. An autonomic response was examined well as environmental conditions. when sighted crayfish (𝑁=5) were placed into the experimental aquarium for interactions. Crayfish pairs were 2.6. Statistical Analysis. Parametric tests (ANOVA and 𝑡 - randomly chosen from the na¨ıve population stock for “in test) were used when comparing differing levels of behavior water” and “out of water” trials. Order of which trials and levels of intensity. When sufficient evidence for nor- occurred first was random. There were multiple days between mality was violated, Mann Whitney Rank Sum was used starting the trials to ensure that social recognition was to compare different experimental conditions on the same unlikely. Craysfi h were wired to record electrocardiograms species. All graphs and statistical tests were performed in (ECGs) for heart rate (HR) [75–77]. In brief, two insulated SigmaPlot Version 11.0 and R 2.15.0 (Systat Software Inc., stainless steel wires (diameter 0.005 inches and with the San Jose, CA, USA). Additional variables were created such coating 0.008 inches; A-M Systems, Carlsborg, WA, USA) as maximum behavior over the 60-minute trial, time to were placed under the dorsal carapace directly over the first maximum behavior observed, the intensity of the rfi st heart 3 days prior to experimentation. Wires were inserted maximum, the number of encounters, number of encounters through holes drilled in the carapace and cemented in place at maximum behavior, and total intensity of all maximum with instant adhesive (Eastman, 5-min drying epoxy). These behavior encounters. two wires were placed to span the heart in a rostral-caudal arrangement to insure an accurate impedance measure dur- ing each heart contraction as shown in Figure 2.Alidwas 3. Results used to prevent the crayfish from exiting the chamber but left a small section uncovered for the wires to exit the chamber 3.1. Social Behavior in Low White Light. Five pairs of sighted anddid notprohibitthe craysfi hfrommovingfreely. All and vfi e pairs of blind craysfi h were allowed to separately physiological measures were recorded though an impedance interact for 60 minutes in low white light (25 lux) to deter- detector which measured dynamic resistance between the mine typical behavioral interactions. For sighted crayfish 6 International Journal of Zoology Table 3: Total number of social interaction across study conditions for sighted crayfish. Social interactions were observed for both “in water” and “out of water.” Each row corresponds to the total number of interactions for a given behavioral score. Each column corresponds to an environmental condition. In this and succeeding tables, the numbers in brackets are the total “out of water” interactions. Behavior Low light Red light No antennules Red light/no antennules ∗∗∗ ∗∗∗ ∗ NS Invasion (1) 183 (120) 101 (77) 47 (54) 54 (58) ∗∗∗ ∗∗ ∗∗∗ ∗∗∗ Touching (2) 160 (97) 107 (120) 98 (135) 70 (99) ∗∗∗ ∗ ∗∗ ∗∗ Acknowledgment (3) 117 (44) 41 (33) 43 (20) 25 (10) ∗∗∗ ∗ ∗ ∗∗∗ Threat display (4) 108 (38) 33 (22) 39 (26) 43 (5) ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ Chase (5) 68 (18) 51 (10) 34 (6) 43 (2) ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ Grasp (6) 49 (2) 63 (5) 31 (2) 13 (2) ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ Dismemberment (7) 27 (0) 20 (2) 8(0) 4 (1) Table 4: Total number of social interaction across study conditions not tail flip and show less intrusion into the conspecifics for blind crayfish. Social interactions were observed both “in water” territory when compared to social interactions in the water and “out of water.” Each row corresponds to the total number of (Figure 5). Blind craysfi h were less responsive to the presence interactions for a given behavioral score. Each column corresponds of conspecifics (fewer interactions), while surface crayfish to an environmental condition. showed an increase in visual displays (possible bluffing mechanism) when interacting out of the water, but failed Red light/no Behavior Low light Red light antennules to escalate the interaction when compared to interaction ∗∗∗ ∗∗∗ ∗∗∗ conducted in the water. u Th s, for both species, out of the Invasion (1) 113 (34) 127 (59) 135 (75) ∗∗∗ ∗∗ ∗ water has the most significant impact on intrinsic behavior Touching (2) 87 (27) 160 (89) 104 (97) and social interactions (Tables 3 and 4). ∗∗∗ ∗∗∗ ∗∗∗ Acknowledgment (3) 60 (5) 65 (6) 93 (22) ANOVA statistical analysis for each environmental con- ∗∗∗ ∗∗∗ ∗∗∗ Threat display (4) 36 (3) 37 (5) 55 (0) dition shows a significant difference between in water and ∗∗∗ ∗∗∗ ∗∗∗ Chase (5) 31 (3) 73 (0) 38 (1) outofwater conditions as indicatedinthe summarytables ∗∗ ∗∗∗ NS Grasp (6) 22 (2) 29 (0) 4(0) (Tables 3 and 4). ANOVA values are as follows: sighted in NS ∗ NS red light (𝐹 = 33.7, 𝑃 < 0.001 ), blind in red light Dismemberment (7) 3 (1) 8(0) 0(0) 13,69 (𝐹 = 17.0,𝑃 < 0.001 ), sighted in white light with no 13,69 antennules (𝐹 = 17.8,𝑃 < 0.001 ), sighted in red light 13,69 in water, they were shown to interact regularly within the with no antennules (𝐹 = 7.588,𝑃 < 0.001 ), and blind 13,69 time period,aswellasescalateininteractionstohighlevels in red light with no antennules (𝐹 = 19.3,𝑃 < 0.001 ). 13,69 of aggression indicated by the total interactions for the eTh refore, interactions occurring out of water showed that behavioral scores (i.e., 6 and 7; Figure 3(a)). Interactions of both species of crayfish were less likely to interact and more sighted craysh fi out of the water were shown to occur less likely to explore their environment. oen, ft and the interactions were shown to be less aggressive due to the few high scores (Figure 3(b)). There are few 3.3. White versus Red Light. A significant difference was interactions overall, for cave crayfish. eTh cave crayfish show found in the number of interactions in blind cave crayfish the same trend in decreasing their interactions out of water (𝑃=0.029) . In general, there were more interactions in red (Figures 4(a) and 4(b)). Both species exhibited significant light than white light for the blind cave crayfish. There was differences in maximum behavior with crayfish in water no significant difference observed for the surface crayfish in being higher than out of water in low light (cave:𝑃=0.031 any type of light. Both species did not exhibit any significant and sighted: 𝑃 < 0.001 ). A similar outcome was found difference in the maximum behavior between white and red forthe totalnumberofinteractionswithinwater being lights. Also, there was no significant difference detected in dominant over out of water (cave:𝑃 = 0.018 and sighted: duration of interactions (Figures 6 and 7). 𝑃 = 0.022 ). On average, sightedcraysfi h hadsignicfi antly In fact, for the red light condition only, there was a more total interactions compared to blind craysfi h in low marginal dieff renceinthe maximumbehavior (𝑃 = 0.056) light(𝑃<0.001) (Figure 5). For either species, there was not for sighted crayfish “in water” having a median value of 7 a significant difference as to when the maximum behavior versus 5“outofwater.” As forthe cave craysfi h, therewas also occurred. er Th e was also no significant difference found in a significant difference in median maximum behavior (6 in the duration of the maximal event or the total duration of all and 3 out)(𝑃 = 0.008) and a signicfi ant difference in the maximal events. median number of interactions in red light (in 104 and out 33)(𝑃=0.0008) . 3.2. Analysis of Varying Environmental Conditions. Analysis of in waterand outofwater treatmentgroupsshowed significant changes in gfi hting strategy due to environmental 3.4. With versus Without Antennules. The cave crayfish had effects. Specifically, out of water results alone or in com- more maximum behavioral encounters without antennules bination with other conditions reveal that both species do than with antennules(𝑃=0.012) . Surface crayfish had more Behavioral score Behavioral score Behavioral score Behavioral score International Journal of Zoology 7 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 1 1 2 20 2 3 3 4 4 5 5 6 6 7 0 7 (a) (b) Figure 3: Comprehensive representation of social interactions for sighted craysfi h in low white light (25 lux). (a) In water. (b) Out of water. A single vertical line indicates a given behavior at a specific point in time as well as the intensity of the behavior. eTh different colored points represent individual pairs in the trials(𝑁=5) . 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 0 30 1 20 2 20 10 3 4 10 7 6 (a) (b) Figure 4: Comprehensive representation of social interactions for cave crayfish in low white light (25 lux). (a) In water. (b) Out of water. A single vertical line indicates a given behavior at a specific point in time as well as the intensity of the behavior. eTh different colored points represent individual pairs in the trials(𝑁=5) . general interactions with antennules rather than without Heart rate (HR) was recorded before, during, and aeft r antennules(𝑃<0.001) . Again, there was no species identified confrontation, plotted for each crayfish during the entire significant difference in maximum behavior over the 60 duration of the trial. A frequency plot of the raw traces shows minutes with or without antennules. dramatic changes in HR during interactions when comparing In red light, the cave crayfish did not show any significant “in water” to “out of water” conditions (Figure 8). Specifically, difference over the 60 minutes in the variables measured. there is a greater u fl ctuation for one individual (most likely However, surface crayfish with antennules had more interac- the subordinate) during and aer ft interactions. As consistent tions over the time period than those without(𝑃=0.039) .In with previously described experiments, it is also shown that low light, the sighted crayfish did show significant difference the “out of water” condition has fewer interactions. eTh raw in the average time to the rfi st maximum behavior (in 9 traces show a rapid response during interactions, especially minutes versus out 19.8 minutes,𝑃=0.012 ). for one individual within a pair, as well as the continued response aer ft the interaction is over. This suggests that “out 3.5. Recording ECGs. The physiological response of crayfish of water” conditions have a greater eeff ct on intrinsic factors, such as HR, for the individuals. This is most apparent for the was recorded to characterize the autonomic response during social interactions as well as for environmental change. individual most likely to become the subordinate since retreat Time (min) Time (min) Time (min) Time (min) Intensity Intensity Intensity Intensity 8 International Journal of Zoology 8 200 4 100 0 0 Cave in Cave out Sight in Sight out Cave in Cave out Sight in Sight out Condition (white light) Condition (white light) (a) (b) Figure 5: Comparison of cave and sighted craysfi h in and out of water in low/white light. (a) eTh mean number of maximum behavior (±SEM) is plotted for the four conditions. There is a significant difference between in and out of water for both species. (b) The mean number of total interactions(±SEM) for the four conditions. er Th e is also a significant decrease in both species between in and out of water in low light. away from the conspecifics is not as feasible out of water and to the chemical cues providing enough information about the thus agreater chance of beingattackedislikelytohappen. environment and the conspecific. The removal of antennules along with red light showed a reduction in the number of interactions but did not diminish the aggression levels since 4. Discussion many of the interactions escalated to a behavioral score of 5 (chase) and 6 (grasp/strike). When these crayfish were taken This study demonstrated that environmental factors directly out of water in combination with the diminished sensory influence crayfish social interactive behavior. Here, we show cues, there was a dramatic decrease in aggression of social that interactions were more aggressive and intense and interaction. This pattern was similar for blind crayfish in more likely to end with a physical confrontation when they red light and the lack of antennules. er Th e were very few took place “in water” compared to “out of water” for two interactions, and the aggression levels were dramatically morphologically and genetically distinct species of crayfish. decreased. Furthermore, heart rate measures during social It is shown that altering environmental conditions induced interactions for a single pair of crayfish showed that “out of crayfish to change their intrinsic behavior which resulted in water” interactions have a large effect on the organism. It is modified social interactions and fighting strategy. For both likely that the dramatic eeff ct on one of the individuals in speciesinlow whitelight andinwater,there wasahigh the pair (most likely the subordinate) is due to an increased value of interactions, and those interactions were likely to probability of injury which could occur in the absence of escalate to higher levels of aggression (behavioural score of water. Although heart rate remained relatively unchanged 5, 6, or 7). eTh duration of interaction was consistently longer when the crayfish were placed into the chamber, heart rate in time (intensity of 0.3 or 0.4) when in water. Interestingly, was shown to immediately decrease for one individual upon when water was removed from the environment, the total interaction with the conspecific. number of interactions, as well as the aggression level and Agonistic behavior is a fundamental factor of ecologi- duration of each interaction, dramatically decreased for both cal nature, and aggression has been studied extensively in species. Across all environmental conditions and exclusion many invertebrate species such as bees [80, 81], ants [82– of sensory systems (i.e., vision and chemosensory), removal 84], termites [85], wasps [86], lobsters [87–90], crabs [91], of water produced the greatest and most consistent change and craysfi h [ 92–94]. Ritualized displays and cues that are in social interactions. For “out of water” trials, both species were shownnot to tail flip(typicalescaperesponse),and they predicative of agonistic success enable the assessment a rivals’ showed less intrusion into the conspecific’s territory as well as relative fighting ability [ 95]. Fights occurring in nature are being less likely to engage in social interactions. Importantly, known to be shorter, less intense, and more likely to end with a tail flip, but the animals do show the fundamental while sighted crayfish did show an increase in visual displays out of the water, a possible bluffing mechanism [ 79], they fight dynamics as seen in laboratory studies [ 96]. Fighting is failed to escalate in social interactions. potentially costly to each contestant for a variety of factors including time and energy [97–101] and physical injuring Interactions in red light for sighted crayfish did not appear to decrease aggression levels. This is most likely due [101–106]. A limited number of studies integrate multiple Average max behavior Average number of interactions Behavioral score Behavioral score Behavioral score Behavioral score Behavioral score Behavioral score International Journal of Zoology 9 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 60 1 20 1 2 2 20 3 3 10 10 5 6 0 7 0 (a) (b) 0.4 0.4 0.3 0.3 0.2 0.2 60 60 0.1 0.1 0 30 20 1 2 20 4 10 6 6 7 0 (c) (d) 0.4 0.4 0.3 0.3 0.2 0.2 60 60 0.1 0.1 50 50 40 40 0 0 30 30 1 1 20 2 20 10 10 5 5 6 6 7 7 0 0 (e) (f) Figure 6: Comprehensive representation of social interactions for sighted crayfish in varying environmental conditions. (a) Red light and in water. (b) Red light and out of water. (c) Low white light, no antennules, and in water. (d) Low white light, no antennules and, out of water. (e) Red light, no antennules and, in water. (f) Red light, no antennules and, out of water. A single vertical line indicates a given behavior at a specific point in time as well as the intensity of the behavior. eTh different colored points represent individual pairs in the trials (𝑁=5) . Time (min) Time (min) Time (min) Time (min) Time (min) Time (min) Intensity Intensity Intensity Intensity Intensity Intensity Behavioral score Behavioral score Behavioral score Behavioral score 10 International Journal of Zoology 0.4 0.4 0.3 0.3 0.2 0.2 0.1 60 50 0.1 0 30 0 30 2 1 0 6 7 0 (a) (b) 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 30 0 20 1 2 20 4 4 5 5 7 0 (c) (d) Figure 7: Comprehensive representation of social interactions for cave crayfish in varying environmental conditions (a) Red light and in water. (b) Red light and out of water. (c) Red light, no antennules and, in water. (d) Red light, no antennules and, out of water. A single vertical line indicates a given behavior at a specific point in time as well as the intensity of the behavior. eTh different colored points represent a total of each individual pairs of crayfish in the trials (𝑁=5) . factors that can influence contest behavior. Details of multiple As expected, behavioral scores incrementally decreased with factor sensory integration for any one species are virtually increasing the aggression levels and duration of interaction, unknown. as the hierarchy is likely established. Observational data The types of behavioral repertories we described are from videoaswellasgraph summariesdocumentthatthe similar to those indexed by Huber and Kravitz [107]inthe interactions do occur throughout the entire hour of the American lobster Homarus americanus and Bergman and observation period. Specifically, interactions are just as likely Moore [96] in two species of crayfish Orconectes rusticus to occur in the last ten minutes as they are in the rfi st ten and Orconectes virilis.However,weusedascaleof0to 7, minutes. So even though a social status is being determined while Bergman and Moore used from(−2) to 5 scale. While within the early interactions, there are continuous bouts the general descriptions were similar for each behavioral to conrfi m or test the opponent within this initial hour of level, there were modified classifications in areas described being introduced. Previous work on the crayfish Astacus in holding an opponent as a “do-see-do,” which relates astacus showed that the number of agonistic challenges, mean to a dance term, where we considered this behavior as a duration, and maximum intensity of encounters, were also dismemberment grasp since they would try to twist the others initially high but then decreased steadily as the hierarchy cheliped off. We also indexed the time of interaction along developed [8]. u Th s, the fact that interactions are still com- with the aggression score and duration so that we could mon aeft r 50 minutes suggest that development of dominance assess over time, the complexity of the repetitive interactions. relationships is incomplete. However, it should be noted Time (min) Time (min) Time (min) Time (min) Intensity Intensity Intensity Intensity International Journal of Zoology 11 0 5 10 15 20 25 30 35 40 45 50 55 60 0 5 10 15 20 25 30 35 40 45 50 55 60 Time (min) Time (min) Crayfish 1 Crayfish 1 Crayfish 2 Crayfish 2 (a) (b) Figure 8: Physiological response of a single pair of crayfish. (a) “In water”. (b) “Out of water”. The dark blue line indicates crayfish one and light blue indicates crayfish two. Each point represents direct counts of each beat over 10-s intervals and then converted to beats per minute (BPM). The red dotted vertical lines indicate a physical interaction. The same pair was used in both conditions with multiple days in between each trial. that a limitation to laboratory studies is the restriction of of craysfi hislikelyamajordrive.Aprevious studyofcave escape from an opponent. This would be less of an issue in crayfish showed this was especially true [ 114, 115]. eTh refore, natural ecosystems; however, small interaction arenas in the animals might be in an anxious state in the conditions of laboratory mayleadtomoreaggressiveinteractions[95, 107]. pairing in this study (new environment), and upon meeting If one were to document the sensory cues necessary for an opponent, they could be hesitant to interact as compared social dominance and maintenance of social hierarchy, a to an intruder invading one’s space when an opponent is more in-depth study is required. In this study, the type of introduced to a resident’s tank. interactions and the effect of environment on these general Studies examining short-term changes in behavior, levels of interactions were the focus. Many observations of specicfi ally social interaction outcomes, have shown that craysfi h behavior have been made to examine specicfi factors physiological changes occur in both learning and the neu- influencing intraspecific aggression such as in shelter acquisi- roendocrine system. The changes in either of these are tion [19, 62, 63], chemical communication [5, 23, 64], mating associated with effects of experience on the neuroendocrine [65], food preferences [66], and starvation [67, 68]. These system of the individuals. Encounter behavior is modified studies provide valuable information to determine intrinsic as a result of learning [116–118]. Learning itself is a physio- and extrinsic factors that affect agonistic interactions. logical change in synaptic transmission in specicfi neuronal There are other extrinsic factors that influence intraspe- pathways. Whether the changes are pre- or postsynaptic cific interactions such as previous history in agonistic is not the issue, but only that physiological changes occur encounters [96, 108, 109], different fighting strategies [ 110], through experience [119]. Neuroendocrine changes such as and prior residence [63, 111]. eTh se can all signica fi ntly impact in corticosteroids and androgens as a relation to fighting the outcome of social interactions. While we cannot control strategy has been well studied in vertebrates [120–126]. The all these factors due to these organisms not being raised relationship between dominance status and corticosteroid exclusively in the lab, we can use craysfi h that have never levels is less clear since in many cases the hormone levels been before placed together into a new environment that is can correlate positively, negatively, or not all with social rank not previously occupied by either in the past. Craysh fi housed as there appears to more of a species specific response [ 126– individually have been shown to be more aggressive [112]and 129]. Serotonin (5-HT) has been associated with aggressive that previous agonistic encounters with the same individuals behavior [88, 130–133]. In invertebrates, increased serotonin can change the outcome of encounters [108, 113]. Since we did shows an increase in aggression [134] since infusion of 5-HT house the crayfish as individuals this might have raised their in the hemocoel cavity of the craysfi h Astacus astacus caused aggressiveness upon interacting. theanimaltofightlongerinanencounter [ 6, 135]. It is most While the use of a new environment will eliminate a prior residence variable, it does still pose other variables likely that aer ft aggressive interactions, further physiological that need to be considered. eTh use of the new environment changes are associated with energy metabolism in modifying introduces the problem of the animals wanting to explore the neuroendocrine system due to energy depletion and hor- the new surroundings and thus could take away interest in monal actions which may even alter synaptic communication the opponent. Searching/exploring behavior for both species [135, 136]. 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Sensory Systems and Environmental Change on Behavior during Social Interactions

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Copyright © 2013 S. M. Bierbower et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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10.1155/2013/573802
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Hindawi Publishing Corporation International Journal of Zoology Volume 2013, Article ID 573802, 16 pages http://dx.doi.org/10.1155/2013/573802 Research Article Sensory Systems and Environmental Change on Behavior during Social Interactions 1 2 1 S. M. Bierbower, J. Nadolski, and R. L. Cooper Department of Biology & Center for Muscle Biology, University of Kentucky, Lexington, KY 40506-0225, USA Department of Mathematical and Computational Sciences, Benedictine University, Lisle, IL 60532, USA Correspondence should be addressed to R. L. Cooper; rlcoop1@email.uky.edu Received 21 December 2012; Revised 13 March 2013; Accepted 15 March 2013 Academic Editor: Randy J. Nelson Copyright © 2013 S. M. Bierbower et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. eTh impact of environmental conditions for transmitting sensory cues and the ability of craysfi h to utilize olfaction and vision were examined in regards to social interactive behavior. eTh duration and intensity of interactions were examined for conspecific crayfish with different sensory abilities. Normally, vision and chemosensory have roles in agonistic communication of Procambarus clarkii; however, for the blind cave crayfish ( Orconectes australis packardi), that lack visual capabilities, olfaction is assumed to be the primary sensory modality. To test this, we paired conspecifics in water and out of water in the presence and absence of white light to examine interactive behaviors when these various sensory modalities are altered. For sighted crayfish, in white light, interactions occurred and escalated; however, when the water was removed, interactions and aggressiveness decreased, but, there was an increase in visual displays out of the water. The loss of olfaction abilities for blind cave and sighted crayfish produced fewer social interactions. The importance of environmental conditions is illustrated for social interactions among sighted and blind crayfish. Importantly, this study shows the relevance in the ecological arena in nature for species survival and how environmental changes disrupt innate behaviors. 1. Introduction established Barnard and Sibly [13] producer-scrounger game in which mixes of strategies work better than all one or Social relationships may take many forms when organisms the other of a specific strategy. er Th e are obvious ecological live in a group, and oen ft times, the individuals must benefits for being the dominant individual and little point in determine their status within a social structure [1–3]. Social interacting if there is an absence of benefits with aggressive dominance is a form of a social relationship in which interactions. us, Th the benefit of interactions must account individuals aggressively interact repeatedly. The interaction not only for the resource, but also the cost in obtaining between individuals is a well-studied sequential series of the resource. The dominate individuals oeft n have increased interactions, with each individual having the option of access to resources such as mates, food, and shelters [14, terminating or continuing the interaction/contest at any time. 15]. However, this may not always be the case since many The consequence of these interactions most likely results other factors play a role such as the value of the resource in a dominant individual who repeatedly wins encounters [16], the inability to monopolize a resource [17], and the against a subordinate [3]. eTh refore, agonistic encounters will loss of resources’ due to stealing of stores/caches by other generally establish social hierarchies between individuals in individuals [18]. Furthermore, females with young often rise apopulation[4–9]. Dominance hierarchies are known to in the social ranks to better provide for their young [19], as decrease aggressive interactions between individuals based well as hungry subordinate individuals oen ft win encounters upon social status, therefore stabilizing the population over against dominants for access to food [20, 21]. time [10, 11]. eTh re are many factors involved in the establishment of Smith [12]suggeststhatrankmay be astrategyindi- social dominance, and it is well documented that environ- viduals adopt to maximize tfi ness in the population based mental cues play a major role in the outcome of social interac- upon theroleofother individuals. Thiscorrelateswiththe tions whether through chemosensory (odors, [22, 23]), visual 2 International Journal of Zoology (opponent posturing, [24, 25]), and/or tactile cues (physical examine whether behavioral, morphological, and/or physio- combat, [4, 5, 7, 8]). logical evolutionary adaptations may have evolved uniquely An ideal model system to study social interactions is with to their species based upon the cave environment. Since crayfish since typical interactions have been well documented cave crayfish have a reduced optic system and have more for decades. Crayfish are known to form social hierarchies olfactory projection neurons than surface sighted crayfish, aer ft very aggressive interactions [ 4–9, 26, 27]. Typically, the it was suggested they have more neural processing related encounters escalate from visual threats of defense postur- to olfaction [39]. Cave craysfi happeartorelyprimarily on ing to actual physical confrontations that include cheliped olfactory and tactile modalities, while surface craysfi h rely grasping andmoreaggressivebehaviors whereone will try primarily on visual and olfactory to assess and monitor to dismember or even kill another individual. their surroundings. Since these cave crayfish do have caudal Currently, most studies observing social interactions photoreceptors in their 6th abdominal ganglion and respond occurinanaturalfieldsiteoralocation that mimics the to white light, studies were performed in white and red typical environment. While this gives insights into typical lights. eTh caudal photoreceptors are not sensitive to the behaviors, little is known of the interaction dynamics when red light used, as assayed in behavioral studies [40]. In naturalchanges occursuchaswhenanorganismleavesthe accordance with the above information, it is logical that cave aquatic environment or when sensory systems are dimin- craysfi h do not show the typical postural behaviors (visual ished. Crayfish leave the water for various reasons such as to display) identified in social encounters within their natural find food, mates, or when excessive competition may drive cave environment. We hypothesized that such displays would them to look for other niches. eTh environmental change not be beneficial since conspecifics are not able to observe with the absence of water would eliminate the typical escape the visual display. While studies have addressed the neural response (i.e., tail flip) which allows for a fast retreat from structure of the optic systems [39]and theeeff ctsoflight on conspecifics. In addition, the absence of water results in other social interactions [40], the typical behaviors of cave crayfish factors influencing social interactions, such as a higher energy have not been as thoroughly studied as with surface crayfish. demand for movement mainly due to the lack of buoyancy, Currently, little is known of interaction dynamics in the a greater probability of injury due to a slower response in absence of water which eliminates the typical escape response movement, as well as retreat and also the lack of assessment (i.e., tail flip) and/or with diminished chemosensory systems through chemical cues of not only conspecifics, but also the in either species of crayfish. environment in general. us, Th an organism is at greater risk Chemical signals are also important sources of informa- since they lack the ability to assess their opponent and/or tion in aquatic environments where visibility maybe limited locate asafeplace forretreat.This is especially true fora when compared to terrestrial open environments [40]. Cray- species evolutionarily lacking a sensory modality. Hence, fish are known to have a [ 41, 42] well-developed olfactory it is of interest to examine the eeff ct of diminished visual system, and studies have shown that chemical signals play and olfactory/chemosensory sensory system. This is possible an important role in many aspects of their life [23, 43, 44]. through studies in the absence of white light and the removal Specifically in agonistic encounters, chemical signals appear of the primary chemosensory appendage (i.e., antennules) in to be more important than other oen ff sive displays and surface species, as well as studies in an evolutionarily distinct signals for settling a gfi ht [ 45]. Interestingly, research has species of crayfish which lack the visual sensory modality. shownthatsomespecies areabletorecognize individuals Although vision and tactile have been suggested to be that they have encountered in the recent past such as two very important in social interactions for mediating the species of hermit crabs [46–48], crab [49], mantis shrimp transfer of information, the full understanding on the ways Gonodactylus festae [50, 51], lobsters Homarus americanus these two sensory cues are used in agonistic communication [52], and crayfish [ 53]. It has been shown that the individual remains unclear. It has been well studied and shown that recognition is based upon chemical signals that are emitted vision is important for agonistic communication in other during social interactions [54–56] in crustaceans [57]. The decapod species, such as dd fi ler crabs [ 28–30], hermit crabs chemical signals are important in maintaining the stable [31–35], lobsters [36], and mantis shrimp [37]. Due to this dominance hierarchies. obvious factor in so many other decapod crustaceans, we Chemical cues are known to be involved in the establish- assume that the visual sensory cue would also be very ment of social hierarchies and are known to impact behavior important for information exchange among crayfish. We [58, 59]. Bovbjerg [5] rfi st suggested that both vision and chose to separate the roles of vision and chemosensory in tactile are involved in the establishment of social hierarchies, the agonistic communication of P. clarkii by conducting and he also demonstrated that antennae are important for experiments in red light (not visible to P. clarkii)aswellas tactile orientation. eTh antennule is considered the organ removing the antennules, both independently and additively most specialized for chemosensory detection and plays a to a red light environment. eTh study of vision in this species leading role in tracking odor plumes [60]and individual is particularly appropriate, given that P. clarkii are normally recognition [61]. One way to address the influence of sensory active under a wide range of environmental light levels, and cues is to remove important sensory systems individually and we mimic periods of dusk and dawn which are known to be simultaneously. Specifically, by removing the antennules and particularly active time points [38]. Blind cave crayfish ( Orconectes australis packardi) lack vision through the absence of white light (provide red light), one can understand the reliance on sensory cues. visual capabilities; therefore, they provide the opportunity to International Journal of Zoology 3 It is apparent that many environmental cues determine the outcome of social interactions. With the assumption that all group members begin with equal gfi hting abilities, environmental eeff cts or diminished sensory cues will most likely disrupt the typical intrinsic behavior. Furthermore, when multiple cues are diminished, the inu fl ence may be additive or behave synergistically in altering a behavior. u Th s, by examining reliance on single sensory systems on well-defined social behavior, we can begin to understand Figure 1: Blind cave crayfish, Orconectes packardi australis,engaged environmental impacts on populations/species. We com- in an agonistic encounter. pared social interactions in white light to experiments in red light to understand the photoreceptors influence on social interactions. 2. Methods Past studies have examined many extrinsic factors that influence intraspecific aggression, such as shelter acquisition 2.1. Animals. Crayfish, Procambarus clarkii (sighted), mea- [19, 62, 63], chemical communication [5, 23, 64], mating suring 5.0–6.25 cm in body length were obtained commer- [65], food preferences [66], and starvation [67, 68]. An area cially (Atchafalaya Biological Supply Co., Raceland, LA, not yet addressed is the extrinsic factor of “out of water” USA). Crayfish, Orconectes australis packardi (Rhoades) (the for crayfish social interactions, and it is unclear whether the blind crayfish), measuring 4.6–6.4 cm, were obtained from hydrodynamics of natural habitats allow for the successful the Sloan’s Valley Cave System near Somerset, KY, USA (state useofchemicalsignals andtypical behavior during social collecting permits were obtained for this study; Figure 1). A interactions in nature. us, Th the purpose of this study is to totalof25sighted and15blind craysfi hwereusedinthe present quantitative analysis of environmental influence on study. Craysfi h pairs were randomly chosen from the na ¨ıve social interactions in two species of crayfish with special population stock. eTh order in which the trials occurred reference to reliance of dieff rent primary sensory modali- was random. No two crayfish were paired together more ties. than once; thus, all encounters were with conspecifics not Intrinsic and extrinsic factors aeff ct intraspecific aggres- previously known to each other. Only male crayfish were sion in many ways, and both should be examined for the used in this study. Animals were housed individually in impact on agonistic behavior. Herein, a simple additive rectangular plastic containers and cared for in the same model for this integration of multiple sensory systems as manner, except for O. a. packardi that were covered with black well as multiple environmental factors in an individual’s plastic to omit light in an aquatic facility within our regulated- expected gfi hting ability determined the impact of additive temperature laboratory (17–20 C). P. clarkii were on a 12- effects. Examination of environmental influence on behavior hour period light-dark cycle. All crayfish were fed dried was through the measure of fighting strategy and intensity fish pellets weekly before and throughout the experiments. of interaction in two species (Procambarus clarkii, sighted Craysfi hhandlingwas conductedbyusing aglass beaker surface crayfish and Orconectes australis packardi, blind cave to transfer crayfish from one container to the another. Due crayfish). to housed containers being cleaned weekly, craysh fi were Due to distinct behavioral, anatomical, biochemical, mor- handled oeft n; the limited handling during experimentation phological, and/or physiological adaptations of cave organ- is assumedtohavelittletonoeeff ct on theinternalstatusof isms, there is a fascination and interest in understanding how the crayfish. Only crayfish in their intermolt stage, possessing they are able to adapt and survive in extreme environments. all walking legs and both chelipeds were used in these studies. Cave crayfish show the general characteristics of anatomical and morphological adaptations of most cave organisms. Specifically when compared to surface crayfish, cave crayfish 2.2. Social Interactions. Initial experiments (i.e., low light) are smaller in size, have longer/thinner appendages, possess were focused on characterizing the general behavioral inter- highly developed nonvisual sensory capabilities, and lack actions for both species of crayfish. Crayfish were randomly pigment and eyes [69]. In addition, behavioral, physio- distributed into fourteen different conditions as discussed logical, and biochemical adaptations have been identified below. Social interactions were staged in size-matched males. in cave crayfish such as a decrease in locomotion and An interaction behavioral scoring index was developed oxygen consumption, as well as a decrease in metabolic (Table 1(a)) for species comparison of P. clarkii and O. rates [70]. eTh se are related to a reduction in energy from australis packardi. Observational preexperimental trials iden- limited food sources and/or oxygen availability in cave tified typical crayfish behavior to establish a quantifiable systems [71–73]. u Th s, these distinct evolutionary adapta- scale for interactions based on both aggressiveness, as well tions allows for studies discerning behavioral differences as intensity (time duration of the interaction, Table 1(b)). in two species of crayfish. Another goal of this study was Craysfi h male pairs of approximate equal size were staged in to identify species-specific behaviors through comparison a glass aquarium and videotaped for one hour, allowing for of cave and a surface species, as well as determining the interaction without outside interference. The crayfish were environmental and olfactory influence on intrinsic behav- monitored indirectly with a TV monitor. Trials conducted iors. in low light in the water served as controls for the sighted 4 International Journal of Zoology Table 1: Social interaction scoring bioindex. (a) Indicates the Most of the general characteristics are previously de- behavioral scoring bioindex used to quantify behavior during each scribedinDingleand Caldwell [74]. Interactions typically trial in the experimental conditions. (b) Indicates the intensity scale began with an invasion of territory or an acknowledgment/ based upon time duration in which the pairs were engaged in a stando.ff Termination of the interaction occurred when the specific behavior. observer determines that individuals no longer appear to be directing behavior at each other. Communication may (a) be occurring,but sincethe purposeofthisstudy was 0 No interaction to concentrate on aggressive interactions, no attempt was 1. Territory invasion made to analyze other possible communicative behaviors. 2. Intentional touching Quantification of behavior was based upon total number of interactions as well as the length of each individual 3. Acknowledgment interaction. 4. Threat display Each trial was critically analyzed to categorize craysfi h 5. Chase behavior, as well as identify general behavioral trends within 6. Grasp/strike and across species. For each environmental condition (i.e., 7. Dismemberment lowlight,red light, andnoantennules),five trials (𝑁 = (b) 5) were runinthe waterand vfi etrials (𝑁 = 5) were run out of the water. All trials were digitally recorded and 0.1 1–15 seconds analyzed through video analysis to record behavioral scores 0.2 16–30 seconds and intensity. To understand behavioral trends, 3D graphs 0.3 31–45 seconds combined all trials together for comparison of the type of 0.4 >45 seconds behavior as well and intensity of each encounter. eTh duration of an interaction was used as a measure of interaction intensity. Since interactions are known to be relatively short, crayfish, while trials conducted in red light in water act atimescale wasused(Table 1(b)). as controls for blind crayfish. The index was then used to quantify each of the trials across conditions and species comparison. Behavioral scores were assigned to pairs of 2.4. Environmental Conditions. The various environmental crayfish (not individual scoring) for every interaction that conditions that were used are listed in Table 2. Social interac- occurred during the 60-minute time period. tions were examined in and out of water in low light (25 lux). “In water” studies used a glass aquarium (20 cm× 10 cm× 2.3. Behavioral Analysis. Previous research and prior obser- 12 cm) 4 cm filled from the top with aerated water. “Out of vation of aggressive interactions between individuals indicate water” studies were conducted using the same aquarium but that the behavior could be classiefi d into several rather dis- without water and still providing wet sand for the animals tinct categories. These categories represent behavior patterns to walk on. “In water” studies (control) for both sighted in what are relatively stereotyped and which are known to and blind crayfish were compared to other environmental be typical behaviors of sighted craysh fi . Brieyfl the behavioral conditions to determine changes in intrinsic behaviors. This acts established are as follows (also see Table 1(a)). part of the study examined: (1) sighted “in water,” (2) sighted “out of water,” (3) blind “in water,” and (4) blind “out of water”. 0-No interaction: no encounter without any evidence Social interactions were also observed in red light. Red of awareness of other individual. lightconditionsusedafilteredred light(2.5Lux)toremove 1-Territory invasion/approach/retreat:deliberate the visual sensory stimulation for the sighted crayfish and the movement towards other individual and a direct, stimulation of the caudal photoreceptors in the cave crayfish. initiation into conspecifics space and/or movement The red light (Kodak Adjustable Safeway Lamp, 15 watts), away. was previously noted to be a wavelength not detected by crayfish [ 9, 40] thus providing no visual sensory stimulation. 2-Intentional touching: a short rapid movement for- The purpose is to examine the reliance of visual cues for ward directed at individual. sighted crayfish out of water when chemosensory cues are 3-Acknowledgment/standoff :facingoneanotherwith- diminished. Furthermore, using blind crayfish in red light out visual threat display. allowed us to help determine if low light induces a stress 4-Meral spread/threat display: outward raising and response that influences social behavior. We examined these spreading of the chelipeds. conditions in this part of the study: (1) sighted/in water/red light, (2) sighted/out of water/red light, (3) blind/in water/red 5-Chase:pursuit aeft r theindividual. light, and (4) blind/out of water/red light (Table 2). 6-Grasp/strike: a blow to or seizing of other individ- The removal of olfactory cues was conducted by removing ual. the antennules (primarily sensory system for chemical detec- 7-Dismemberment:veryaggressiveactiontoindivid- tion) with sharp scissors at the base of the antennules by the ual in which dismemberment or likelihood of killing first annuli. er Th e was no death associated with antennulec- is apparent. tomy as this is not that invasive of a surgery for crayfish. In International Journal of Zoology 5 Table 2: Social interaction conditions for both species of crayfish. Social interactions were observed both in and out of the water for sighted and blind crayfish. Assessment of different sensory modalities impact on intrinsic behavior was examined through methodical removal of one or many sensory cues. Sighted Blind In water Out of water In water Out of water Low light Low light Low light Low light Red light Red light Red light Red light Low light/no Low light/no —— antennules antennules Red light/no Red light/no Red light/no Red light/no Figure 2: Schematic representation for the placement of the record- ing wires for monitoring the heart from a crayfish (Procambarus antennules antennules antennules antennules clarkii.). On the dorsal carapace, large arrows represent the two wires which spanned the rostral-caudal axis of the heart to monitor any change in the dynamic resistance, which is used as a measure of heart fact, there is little blood loss as well since this is not that wide rate. of a region as compared to the very base of the antennules next to the cephalothorax. eTh animals were held for 3 days for recovery aeft r antennulectomy. “In water” and “out of stainless steel wires and recorded on-line to a PowerLab via water” studies were again conducted for both species of cray- a PowerLab/4SP interface (AD Instruments). All events were fish. The purpose of removing the antennules was to further measured andcalibratedwiththe PowerLab Chartsoftware understand the reliance of visual cues for sighted crayfish and version 5.5.6 (AD Instruments, Australia). Previous studies to understand impacts on social behavior for blind craysfi h if showed that 3 days was enough time for the animals to there was a lack of environmental olfactory cues. These set return to physiological measurements similar to levels prior of conditions compared (1) sighted/in water/no antennules, to handling [78]. Cave crayfish typically have a thinner, more (2) sighted/out of water/no antennules, (3) blind/in water/no brittle exoskeleton resulting in more delicate handling during antennules, and (4) blind/out of water/no antennules. wiring. To determine the reliance on environmental cues during Analysis of the response consisted of heart rate in social interactions for sighted crayfish, both chemosensory beats per minute (BPM). HR was monitored in and out of and visual cues were removed. Social interactions were water under control conditions to determine physiological examined for sighted crayfish only in red light and with responses during social interactions. This provided an inter- the removal of antennules in order to compare these two nal measure to external cues. The experimental procedure conditions: (1) sighted/in water/red light/no antennules and consisted HR recordings before, during, and after social (2) sighted/out of water/red light/no antennules. interactions. HR was analyzed to provide a BPM to note changesinthe internal response baseduponinteractions, as 2.5. Recording ECGs. An autonomic response was examined well as environmental conditions. when sighted crayfish (𝑁=5) were placed into the experimental aquarium for interactions. Crayfish pairs were 2.6. Statistical Analysis. Parametric tests (ANOVA and 𝑡 - randomly chosen from the na¨ıve population stock for “in test) were used when comparing differing levels of behavior water” and “out of water” trials. Order of which trials and levels of intensity. When sufficient evidence for nor- occurred first was random. There were multiple days between mality was violated, Mann Whitney Rank Sum was used starting the trials to ensure that social recognition was to compare different experimental conditions on the same unlikely. Craysfi h were wired to record electrocardiograms species. All graphs and statistical tests were performed in (ECGs) for heart rate (HR) [75–77]. In brief, two insulated SigmaPlot Version 11.0 and R 2.15.0 (Systat Software Inc., stainless steel wires (diameter 0.005 inches and with the San Jose, CA, USA). Additional variables were created such coating 0.008 inches; A-M Systems, Carlsborg, WA, USA) as maximum behavior over the 60-minute trial, time to were placed under the dorsal carapace directly over the first maximum behavior observed, the intensity of the rfi st heart 3 days prior to experimentation. Wires were inserted maximum, the number of encounters, number of encounters through holes drilled in the carapace and cemented in place at maximum behavior, and total intensity of all maximum with instant adhesive (Eastman, 5-min drying epoxy). These behavior encounters. two wires were placed to span the heart in a rostral-caudal arrangement to insure an accurate impedance measure dur- ing each heart contraction as shown in Figure 2.Alidwas 3. Results used to prevent the crayfish from exiting the chamber but left a small section uncovered for the wires to exit the chamber 3.1. Social Behavior in Low White Light. Five pairs of sighted anddid notprohibitthe craysfi hfrommovingfreely. All and vfi e pairs of blind craysfi h were allowed to separately physiological measures were recorded though an impedance interact for 60 minutes in low white light (25 lux) to deter- detector which measured dynamic resistance between the mine typical behavioral interactions. For sighted crayfish 6 International Journal of Zoology Table 3: Total number of social interaction across study conditions for sighted crayfish. Social interactions were observed for both “in water” and “out of water.” Each row corresponds to the total number of interactions for a given behavioral score. Each column corresponds to an environmental condition. In this and succeeding tables, the numbers in brackets are the total “out of water” interactions. Behavior Low light Red light No antennules Red light/no antennules ∗∗∗ ∗∗∗ ∗ NS Invasion (1) 183 (120) 101 (77) 47 (54) 54 (58) ∗∗∗ ∗∗ ∗∗∗ ∗∗∗ Touching (2) 160 (97) 107 (120) 98 (135) 70 (99) ∗∗∗ ∗ ∗∗ ∗∗ Acknowledgment (3) 117 (44) 41 (33) 43 (20) 25 (10) ∗∗∗ ∗ ∗ ∗∗∗ Threat display (4) 108 (38) 33 (22) 39 (26) 43 (5) ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ Chase (5) 68 (18) 51 (10) 34 (6) 43 (2) ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ Grasp (6) 49 (2) 63 (5) 31 (2) 13 (2) ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ Dismemberment (7) 27 (0) 20 (2) 8(0) 4 (1) Table 4: Total number of social interaction across study conditions not tail flip and show less intrusion into the conspecifics for blind crayfish. Social interactions were observed both “in water” territory when compared to social interactions in the water and “out of water.” Each row corresponds to the total number of (Figure 5). Blind craysfi h were less responsive to the presence interactions for a given behavioral score. Each column corresponds of conspecifics (fewer interactions), while surface crayfish to an environmental condition. showed an increase in visual displays (possible bluffing mechanism) when interacting out of the water, but failed Red light/no Behavior Low light Red light antennules to escalate the interaction when compared to interaction ∗∗∗ ∗∗∗ ∗∗∗ conducted in the water. u Th s, for both species, out of the Invasion (1) 113 (34) 127 (59) 135 (75) ∗∗∗ ∗∗ ∗ water has the most significant impact on intrinsic behavior Touching (2) 87 (27) 160 (89) 104 (97) and social interactions (Tables 3 and 4). ∗∗∗ ∗∗∗ ∗∗∗ Acknowledgment (3) 60 (5) 65 (6) 93 (22) ANOVA statistical analysis for each environmental con- ∗∗∗ ∗∗∗ ∗∗∗ Threat display (4) 36 (3) 37 (5) 55 (0) dition shows a significant difference between in water and ∗∗∗ ∗∗∗ ∗∗∗ Chase (5) 31 (3) 73 (0) 38 (1) outofwater conditions as indicatedinthe summarytables ∗∗ ∗∗∗ NS Grasp (6) 22 (2) 29 (0) 4(0) (Tables 3 and 4). ANOVA values are as follows: sighted in NS ∗ NS red light (𝐹 = 33.7, 𝑃 < 0.001 ), blind in red light Dismemberment (7) 3 (1) 8(0) 0(0) 13,69 (𝐹 = 17.0,𝑃 < 0.001 ), sighted in white light with no 13,69 antennules (𝐹 = 17.8,𝑃 < 0.001 ), sighted in red light 13,69 in water, they were shown to interact regularly within the with no antennules (𝐹 = 7.588,𝑃 < 0.001 ), and blind 13,69 time period,aswellasescalateininteractionstohighlevels in red light with no antennules (𝐹 = 19.3,𝑃 < 0.001 ). 13,69 of aggression indicated by the total interactions for the eTh refore, interactions occurring out of water showed that behavioral scores (i.e., 6 and 7; Figure 3(a)). Interactions of both species of crayfish were less likely to interact and more sighted craysh fi out of the water were shown to occur less likely to explore their environment. oen, ft and the interactions were shown to be less aggressive due to the few high scores (Figure 3(b)). There are few 3.3. White versus Red Light. A significant difference was interactions overall, for cave crayfish. eTh cave crayfish show found in the number of interactions in blind cave crayfish the same trend in decreasing their interactions out of water (𝑃=0.029) . In general, there were more interactions in red (Figures 4(a) and 4(b)). Both species exhibited significant light than white light for the blind cave crayfish. There was differences in maximum behavior with crayfish in water no significant difference observed for the surface crayfish in being higher than out of water in low light (cave:𝑃=0.031 any type of light. Both species did not exhibit any significant and sighted: 𝑃 < 0.001 ). A similar outcome was found difference in the maximum behavior between white and red forthe totalnumberofinteractionswithinwater being lights. Also, there was no significant difference detected in dominant over out of water (cave:𝑃 = 0.018 and sighted: duration of interactions (Figures 6 and 7). 𝑃 = 0.022 ). On average, sightedcraysfi h hadsignicfi antly In fact, for the red light condition only, there was a more total interactions compared to blind craysfi h in low marginal dieff renceinthe maximumbehavior (𝑃 = 0.056) light(𝑃<0.001) (Figure 5). For either species, there was not for sighted crayfish “in water” having a median value of 7 a significant difference as to when the maximum behavior versus 5“outofwater.” As forthe cave craysfi h, therewas also occurred. er Th e was also no significant difference found in a significant difference in median maximum behavior (6 in the duration of the maximal event or the total duration of all and 3 out)(𝑃 = 0.008) and a signicfi ant difference in the maximal events. median number of interactions in red light (in 104 and out 33)(𝑃=0.0008) . 3.2. Analysis of Varying Environmental Conditions. Analysis of in waterand outofwater treatmentgroupsshowed significant changes in gfi hting strategy due to environmental 3.4. With versus Without Antennules. The cave crayfish had effects. Specifically, out of water results alone or in com- more maximum behavioral encounters without antennules bination with other conditions reveal that both species do than with antennules(𝑃=0.012) . Surface crayfish had more Behavioral score Behavioral score Behavioral score Behavioral score International Journal of Zoology 7 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 1 1 2 20 2 3 3 4 4 5 5 6 6 7 0 7 (a) (b) Figure 3: Comprehensive representation of social interactions for sighted craysfi h in low white light (25 lux). (a) In water. (b) Out of water. A single vertical line indicates a given behavior at a specific point in time as well as the intensity of the behavior. eTh different colored points represent individual pairs in the trials(𝑁=5) . 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 0 30 1 20 2 20 10 3 4 10 7 6 (a) (b) Figure 4: Comprehensive representation of social interactions for cave crayfish in low white light (25 lux). (a) In water. (b) Out of water. A single vertical line indicates a given behavior at a specific point in time as well as the intensity of the behavior. eTh different colored points represent individual pairs in the trials(𝑁=5) . general interactions with antennules rather than without Heart rate (HR) was recorded before, during, and aeft r antennules(𝑃<0.001) . Again, there was no species identified confrontation, plotted for each crayfish during the entire significant difference in maximum behavior over the 60 duration of the trial. A frequency plot of the raw traces shows minutes with or without antennules. dramatic changes in HR during interactions when comparing In red light, the cave crayfish did not show any significant “in water” to “out of water” conditions (Figure 8). Specifically, difference over the 60 minutes in the variables measured. there is a greater u fl ctuation for one individual (most likely However, surface crayfish with antennules had more interac- the subordinate) during and aer ft interactions. As consistent tions over the time period than those without(𝑃=0.039) .In with previously described experiments, it is also shown that low light, the sighted crayfish did show significant difference the “out of water” condition has fewer interactions. eTh raw in the average time to the rfi st maximum behavior (in 9 traces show a rapid response during interactions, especially minutes versus out 19.8 minutes,𝑃=0.012 ). for one individual within a pair, as well as the continued response aer ft the interaction is over. This suggests that “out 3.5. Recording ECGs. The physiological response of crayfish of water” conditions have a greater eeff ct on intrinsic factors, such as HR, for the individuals. This is most apparent for the was recorded to characterize the autonomic response during social interactions as well as for environmental change. individual most likely to become the subordinate since retreat Time (min) Time (min) Time (min) Time (min) Intensity Intensity Intensity Intensity 8 International Journal of Zoology 8 200 4 100 0 0 Cave in Cave out Sight in Sight out Cave in Cave out Sight in Sight out Condition (white light) Condition (white light) (a) (b) Figure 5: Comparison of cave and sighted craysfi h in and out of water in low/white light. (a) eTh mean number of maximum behavior (±SEM) is plotted for the four conditions. There is a significant difference between in and out of water for both species. (b) The mean number of total interactions(±SEM) for the four conditions. er Th e is also a significant decrease in both species between in and out of water in low light. away from the conspecifics is not as feasible out of water and to the chemical cues providing enough information about the thus agreater chance of beingattackedislikelytohappen. environment and the conspecific. The removal of antennules along with red light showed a reduction in the number of interactions but did not diminish the aggression levels since 4. Discussion many of the interactions escalated to a behavioral score of 5 (chase) and 6 (grasp/strike). When these crayfish were taken This study demonstrated that environmental factors directly out of water in combination with the diminished sensory influence crayfish social interactive behavior. Here, we show cues, there was a dramatic decrease in aggression of social that interactions were more aggressive and intense and interaction. This pattern was similar for blind crayfish in more likely to end with a physical confrontation when they red light and the lack of antennules. er Th e were very few took place “in water” compared to “out of water” for two interactions, and the aggression levels were dramatically morphologically and genetically distinct species of crayfish. decreased. Furthermore, heart rate measures during social It is shown that altering environmental conditions induced interactions for a single pair of crayfish showed that “out of crayfish to change their intrinsic behavior which resulted in water” interactions have a large effect on the organism. It is modified social interactions and fighting strategy. For both likely that the dramatic eeff ct on one of the individuals in speciesinlow whitelight andinwater,there wasahigh the pair (most likely the subordinate) is due to an increased value of interactions, and those interactions were likely to probability of injury which could occur in the absence of escalate to higher levels of aggression (behavioural score of water. Although heart rate remained relatively unchanged 5, 6, or 7). eTh duration of interaction was consistently longer when the crayfish were placed into the chamber, heart rate in time (intensity of 0.3 or 0.4) when in water. Interestingly, was shown to immediately decrease for one individual upon when water was removed from the environment, the total interaction with the conspecific. number of interactions, as well as the aggression level and Agonistic behavior is a fundamental factor of ecologi- duration of each interaction, dramatically decreased for both cal nature, and aggression has been studied extensively in species. Across all environmental conditions and exclusion many invertebrate species such as bees [80, 81], ants [82– of sensory systems (i.e., vision and chemosensory), removal 84], termites [85], wasps [86], lobsters [87–90], crabs [91], of water produced the greatest and most consistent change and craysfi h [ 92–94]. Ritualized displays and cues that are in social interactions. For “out of water” trials, both species were shownnot to tail flip(typicalescaperesponse),and they predicative of agonistic success enable the assessment a rivals’ showed less intrusion into the conspecific’s territory as well as relative fighting ability [ 95]. Fights occurring in nature are being less likely to engage in social interactions. Importantly, known to be shorter, less intense, and more likely to end with a tail flip, but the animals do show the fundamental while sighted crayfish did show an increase in visual displays out of the water, a possible bluffing mechanism [ 79], they fight dynamics as seen in laboratory studies [ 96]. Fighting is failed to escalate in social interactions. potentially costly to each contestant for a variety of factors including time and energy [97–101] and physical injuring Interactions in red light for sighted crayfish did not appear to decrease aggression levels. This is most likely due [101–106]. A limited number of studies integrate multiple Average max behavior Average number of interactions Behavioral score Behavioral score Behavioral score Behavioral score Behavioral score Behavioral score International Journal of Zoology 9 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 60 1 20 1 2 2 20 3 3 10 10 5 6 0 7 0 (a) (b) 0.4 0.4 0.3 0.3 0.2 0.2 60 60 0.1 0.1 0 30 20 1 2 20 4 10 6 6 7 0 (c) (d) 0.4 0.4 0.3 0.3 0.2 0.2 60 60 0.1 0.1 50 50 40 40 0 0 30 30 1 1 20 2 20 10 10 5 5 6 6 7 7 0 0 (e) (f) Figure 6: Comprehensive representation of social interactions for sighted crayfish in varying environmental conditions. (a) Red light and in water. (b) Red light and out of water. (c) Low white light, no antennules, and in water. (d) Low white light, no antennules and, out of water. (e) Red light, no antennules and, in water. (f) Red light, no antennules and, out of water. A single vertical line indicates a given behavior at a specific point in time as well as the intensity of the behavior. eTh different colored points represent individual pairs in the trials (𝑁=5) . Time (min) Time (min) Time (min) Time (min) Time (min) Time (min) Intensity Intensity Intensity Intensity Intensity Intensity Behavioral score Behavioral score Behavioral score Behavioral score 10 International Journal of Zoology 0.4 0.4 0.3 0.3 0.2 0.2 0.1 60 50 0.1 0 30 0 30 2 1 0 6 7 0 (a) (b) 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 30 0 20 1 2 20 4 4 5 5 7 0 (c) (d) Figure 7: Comprehensive representation of social interactions for cave crayfish in varying environmental conditions (a) Red light and in water. (b) Red light and out of water. (c) Red light, no antennules and, in water. (d) Red light, no antennules and, out of water. A single vertical line indicates a given behavior at a specific point in time as well as the intensity of the behavior. eTh different colored points represent a total of each individual pairs of crayfish in the trials (𝑁=5) . factors that can influence contest behavior. Details of multiple As expected, behavioral scores incrementally decreased with factor sensory integration for any one species are virtually increasing the aggression levels and duration of interaction, unknown. as the hierarchy is likely established. Observational data The types of behavioral repertories we described are from videoaswellasgraph summariesdocumentthatthe similar to those indexed by Huber and Kravitz [107]inthe interactions do occur throughout the entire hour of the American lobster Homarus americanus and Bergman and observation period. Specifically, interactions are just as likely Moore [96] in two species of crayfish Orconectes rusticus to occur in the last ten minutes as they are in the rfi st ten and Orconectes virilis.However,weusedascaleof0to 7, minutes. So even though a social status is being determined while Bergman and Moore used from(−2) to 5 scale. While within the early interactions, there are continuous bouts the general descriptions were similar for each behavioral to conrfi m or test the opponent within this initial hour of level, there were modified classifications in areas described being introduced. Previous work on the crayfish Astacus in holding an opponent as a “do-see-do,” which relates astacus showed that the number of agonistic challenges, mean to a dance term, where we considered this behavior as a duration, and maximum intensity of encounters, were also dismemberment grasp since they would try to twist the others initially high but then decreased steadily as the hierarchy cheliped off. We also indexed the time of interaction along developed [8]. u Th s, the fact that interactions are still com- with the aggression score and duration so that we could mon aeft r 50 minutes suggest that development of dominance assess over time, the complexity of the repetitive interactions. relationships is incomplete. However, it should be noted Time (min) Time (min) Time (min) Time (min) Intensity Intensity Intensity Intensity International Journal of Zoology 11 0 5 10 15 20 25 30 35 40 45 50 55 60 0 5 10 15 20 25 30 35 40 45 50 55 60 Time (min) Time (min) Crayfish 1 Crayfish 1 Crayfish 2 Crayfish 2 (a) (b) Figure 8: Physiological response of a single pair of crayfish. (a) “In water”. (b) “Out of water”. The dark blue line indicates crayfish one and light blue indicates crayfish two. Each point represents direct counts of each beat over 10-s intervals and then converted to beats per minute (BPM). The red dotted vertical lines indicate a physical interaction. The same pair was used in both conditions with multiple days in between each trial. that a limitation to laboratory studies is the restriction of of craysfi hislikelyamajordrive.Aprevious studyofcave escape from an opponent. This would be less of an issue in crayfish showed this was especially true [ 114, 115]. eTh refore, natural ecosystems; however, small interaction arenas in the animals might be in an anxious state in the conditions of laboratory mayleadtomoreaggressiveinteractions[95, 107]. pairing in this study (new environment), and upon meeting If one were to document the sensory cues necessary for an opponent, they could be hesitant to interact as compared social dominance and maintenance of social hierarchy, a to an intruder invading one’s space when an opponent is more in-depth study is required. In this study, the type of introduced to a resident’s tank. interactions and the effect of environment on these general Studies examining short-term changes in behavior, levels of interactions were the focus. Many observations of specicfi ally social interaction outcomes, have shown that craysfi h behavior have been made to examine specicfi factors physiological changes occur in both learning and the neu- influencing intraspecific aggression such as in shelter acquisi- roendocrine system. The changes in either of these are tion [19, 62, 63], chemical communication [5, 23, 64], mating associated with effects of experience on the neuroendocrine [65], food preferences [66], and starvation [67, 68]. These system of the individuals. Encounter behavior is modified studies provide valuable information to determine intrinsic as a result of learning [116–118]. Learning itself is a physio- and extrinsic factors that affect agonistic interactions. logical change in synaptic transmission in specicfi neuronal There are other extrinsic factors that influence intraspe- pathways. Whether the changes are pre- or postsynaptic cific interactions such as previous history in agonistic is not the issue, but only that physiological changes occur encounters [96, 108, 109], different fighting strategies [ 110], through experience [119]. Neuroendocrine changes such as and prior residence [63, 111]. eTh se can all signica fi ntly impact in corticosteroids and androgens as a relation to fighting the outcome of social interactions. While we cannot control strategy has been well studied in vertebrates [120–126]. The all these factors due to these organisms not being raised relationship between dominance status and corticosteroid exclusively in the lab, we can use craysfi h that have never levels is less clear since in many cases the hormone levels been before placed together into a new environment that is can correlate positively, negatively, or not all with social rank not previously occupied by either in the past. Craysh fi housed as there appears to more of a species specific response [ 126– individually have been shown to be more aggressive [112]and 129]. Serotonin (5-HT) has been associated with aggressive that previous agonistic encounters with the same individuals behavior [88, 130–133]. In invertebrates, increased serotonin can change the outcome of encounters [108, 113]. Since we did shows an increase in aggression [134] since infusion of 5-HT house the crayfish as individuals this might have raised their in the hemocoel cavity of the craysfi h Astacus astacus caused aggressiveness upon interacting. theanimaltofightlongerinanencounter [ 6, 135]. It is most While the use of a new environment will eliminate a prior residence variable, it does still pose other variables likely that aer ft aggressive interactions, further physiological that need to be considered. eTh use of the new environment changes are associated with energy metabolism in modifying introduces the problem of the animals wanting to explore the neuroendocrine system due to energy depletion and hor- the new surroundings and thus could take away interest in monal actions which may even alter synaptic communication the opponent. Searching/exploring behavior for both species [135, 136]. 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