Abstract
Environmental cues contain critical information for individuals while searching for mates and suitable habitat. Crayfish have well-developed chemosensory abilities for detecting environmental cues in water; much less is known about these abilities on land. The Devil crayfish (Cambarus diogenes) is a burrowing crayfish often found in dense floodplain colonies as adults. Juveniles however are released in surface water and must navigate overland to burrow. Previous work demonstrates juveniles use cues from conspecific adults, and to a lesser extent, soil cues, for burrow site selection. Using mesocosms, we build on this by examining burrowing cues associated with (1) congeneric adults, (2) excavated burrow material and (3) other juveniles. In contrast to conspecific adults, cues provided by congeneric adults did not override cues associated with soil type. Similarly, juveniles burrowed closer to conspecific adult burrow mounds than to congeneric and human-built mounds. Juveniles also showed significant grouping behaviour in the absence of all other cues. These results suggest juvenile crayfish integrate multiple terrestrial cues for burrow site selection.
1. Introduction
The factors regulating populations are a function of multiple interacting local and regional phenomena broadly explained by adult fecundity and mortality as well as juvenile survivorship and recruitment (Berven, 1990; Murdoch, 1994; Rodenhouse et al., 1997). Perhaps less obvious, navigation, migration, and other movements are important factors in population regulation as they aid in detection of home ranges, optimal habitats, and mating opportunities (Kamran & Moore, 2015). More specifically, success of juveniles finding and occupying critical habitat is essential for population viability; however, complex life cycles can limit successful juvenile recruitment in some species (Wilbur, 1980; Berven, 1990; Schmidt et al., 2012). Thus, it is important that species use cues from their environment that are reliably effective and capable of discerning true signal from environmental noise and turbulence.
Environmental cues used for navigation, migration, orientation, and homing vary across taxa. For example, desert ants (Cataglyphis fortis) use olfactory cues to return to their burrows after foraging (Bühlmann et al., 2012), honey bees (Apis mellifera) and several ant species (Formicidae) use landmarks associated with previously travelled routes (Hölldobler, 1974; Menzel et al., 1998; Bühlmann et al., 2011), and juvenile loggerhead sea turtles (Caretta caretta) use gravitational cues for migration and feeding (Avens, 2004). Additionally, there is evidence that navigating in groups (‘many-wrongs principle’) is more advantageous than individual navigation due to suppression of individual error by group cohesion (Simons, 2004; Codling et al., 2007). Crustaceans use a particularly diverse set of environmental cues to aid in navigation, migration, and orientation, largely due to a wide range in patterns and scales of mobility across species (Zeil & Hemmi, 2006; Walls & Layne, 2009). Several groups of crustaceans, including amphipods, isopods, and spiny lobsters can orient to the Earth’s geomagnetic field (Lohmann & Ernst, 2014). Crayfish use a range of chemical and sensory cues to find food, mates, and potential competitors (Thorp & Ammerman, 1978; Basil & Sandeman, 2000; Keller et al., 2001; Corotto & O’Brien, 2002). Recent studies also suggest that crayfish are capable of homing behaviours (Kamran & Moore, 2015), but whether or not this involves a combination of navigational cues and group migration is not yet understood.
Understanding factors driving size and stability of crayfish populations is particularly important because these animals play a key role in aquatic and terrestrial food webs, linking several different trophic levels. They are prey for fish (Stein, 1977; Garvey et al., 1994; Adams, 2007), birds (Kushlan, 1986) and mammals (Englund & Krupa, 2000), but also serve as predators, herbivores, detritivores and scavengers (Heard & Richardson, 1995; Nyström et al., 1996; Taylor et al., 2007). They are important geomorphic agents, altering aquatic and terrestrial ecosystems through sediment processing, bioturbation, and burrowing (Statzner et al., 2000; Butler, 2002; Creed & Reed, 2004; Helms & Creed, 2005). Crayfish species vary in their capacity for burrowing and in their ultimate use of burrows (Hobbs, 1981; Berrill & Chenoweth, 1982; DiStefano et al., 2009). Many burrowing crayfish species tend to exhibit strong spatial clumping, which is partly a function of abiotic factors, such as local soil, hydrologic and geomorphologic conditions (Grow, 1982; Loughman et al., 2012; Helms et al., 2013a). However, the degree of connectivity between spatially segregated burrowing populations, and the specific cues and movement patterns used by these animals as they navigate the terrestrial landscape, is largely unknown.
Cambarus diogenes (Devil crayfish) is a burrowing crayfish widely-distributed alongside streams, rivers and ponds across Eastern North America (Grow, 1981; Taylor et al., 2007; Helms et al., 2013a). It inhabits flood plains and seasonally flooded woodland areas, constructing elaborate burrow systems usually topped with well-constructed earthen mounds (‘chimneys’ see also Grow, 1982; Helms et al., 2013a). Female C. diogenes generally leave terrestrial burrows and enter nearby surface waters to release their young during winter and early spring (Hobbs, 1981; Pflieger & Dryden, 1996). After a period of development and growth in surface waters, juveniles return to terrestrial habitats. Juvenile burrows are abundant in stream margins by mid-summer with adult burrows active in the floodplain early spring through fall (Pflieger & Dryden, 1996; Helms et al., 2013a). Thus accurate navigation from an aquatic environment to terrestrial burrowing habitat containing suitable soil, groundwater and foraging conditions, as well as potential mates, is necessary to maintain population viability. Previous studies with C. diogenes suggest that isolated juveniles prefer clayey, floodplain soils over sandy, streamside soils for burrowing; in the presence of conspecific adults however, juveniles prefer adult burrowing locations irrespective of soil type (Grow, 1982; Helms et al., 2013a). In this study, we investigate further potential drivers of observed burrowing distributions by addressing the following questions:
(1) Are juveniles attracted to burrows near congeneric adults in the same manner as previously demonstrated for conspecific adults?
(2) Do adult burrow mounds serve as an important cue for juvenile site selection?
(3) Do juveniles display group behavior when searching for burrow sites?
Prior studies using Fallicambarus fodiens (Trepanier & Dunham, 1999; Punzalen et al., 2001) collectively have shown chimneys act as cues for conspecifics and adults can discriminate conspecific-built and human-built chimneys. Building on these findings, we predicted that C. diogenes juveniles would burrow in areas with congeneric adult chimneys over areas that contained no chimney cue, and when provided a choice, juveniles would burrow near conspecific adult chimneys over congeneric chimneys. We also predicted that, based on prior studies of conspecific tolerances of burrowing crayfish (Dalosto et al., 2013; Helms et al., 2013b), juveniles would group when selecting sites for initial burrows.
2. Methods
2.1. Study animals
All crayfishes used were collected from tributaries of the Tallapoosa River basin in east Alabama, USA. Adult C. diogenes (mean carapace length (CL) ± SD 36.45 ± 3.15 mm) were collected via burrow excavation in the flood plains of Choctafaula Creek and Odum Creek, Macon County, AL, USA. Cambarus striatus (Ambiguous crayfish) and C. latimanus (Variable crayfish), closely-related species often occurring in the same open water and burrowing habitats as C. diogenes (MC personal observation), were used as congeneric outgroups in study trials. Although both C. latimanus and C. striatus are recognized species, they often strongly overlap in habitat and physical characters (Bouchard, 1978; Hobbs, 1981), thus were considered ecological equivalents for this effort. Adult C. striatus (CL 43.61 ± 5.13 mm) were collected from Odum Creek and adult C. latimanus (CL 33.40 ± 6.02 mm) were collected from Choctafaula Creek in Spring 2013. Juvenile C. diogenes were hatched from a berried female collected from Odum Creek and reared in a flow-through pond water trough until they had attained an average CL of 16.77 ± 1.04 mm, sexes indistinguishable. Adults were housed separately from juveniles in species-specific flow-through tanks containing PVC refugia prior to experimentation at the South Auburn Fisheries Research Station, Auburn, AL, USA.
A schematic and photograph of an artificial burrowing chamber (ABC) used to manipulate soil preferences and congeneric cues. Arrows in schematic denote water flow. The ABC was constructed of acrylic, was 30 cm H × 46 cm L × 5 cm W and filled with streamside soil on one side and floodplain soil on the other. Adult crayfish were constrained to burrow in one soil treatment, and juveniles were placed on soil midline and allowed to burrow.
Citation: Behaviour 154, 12 (2017) ; 10.1163/1568539X-00003463
A schematic and photograph of an artificial burrowing chamber (ABC) used to manipulate soil preferences and congeneric cues. Arrows in schematic denote water flow. The ABC was constructed of acrylic, was 30 cm H × 46 cm L × 5 cm W and filled with streamside soil on one side and floodplain soil on the other. Adult crayfish were constrained to burrow in one soil treatment, and juveniles were placed on soil midline and allowed to burrow.
Citation: Behaviour 154, 12 (2017) ; 10.1163/1568539X-00003463
A schematic and photograph of an artificial burrowing chamber (ABC) used to manipulate soil preferences and congeneric cues. Arrows in schematic denote water flow. The ABC was constructed of acrylic, was 30 cm H × 46 cm L × 5 cm W and filled with streamside soil on one side and floodplain soil on the other. Adult crayfish were constrained to burrow in one soil treatment, and juveniles were placed on soil midline and allowed to burrow.
Citation: Behaviour 154, 12 (2017) ; 10.1163/1568539X-00003463
2.2. Experiment 1: effects of congeneric adults on site selection
We used artificial burrowing chambers (ABCs, Figure 1; Stoeckel et al., 2011) to test whether presence of a congeneric adult influenced juvenile burrow site selection in a similar manner as reported in Helms et al. (2013a) for conspecific adults. Chambers measured 30 cm H × 46 cm L × 5 cm W. They were laterally bisected with a removable plastic divider, filled with clayey floodplain soils in one-half and sandy streamside soils in the other half, and the plastic divider subsequently removed (Figure 1). A single adult C. latimanus was placed in each of 10 chambers and constrained to burrow in either streamside or floodplain soils (5 chambers per soil designation). After the adults burrowed (usually within 24 h), one juvenile C. diogenes was placed on the centre line and allowed to burrow (Figure 1). After juveniles burrowed (usually within 8 h), we recorded soil type of the juvenile burrow location and used Pearson’s test to test for departures from random across all chambers.
2.3. Experiment 2: effect of soil mound source on juvenile burrow location
To test whether the source of burrow mounds influenced location of juvenile burrows, we exposed juvenile C. diogenes simultaneously to mounds constructed by a conspecific adult, a congeneric adult (C. striatus) and a human. Adult crayfish mounds were obtained by allowing 10 C. diogenes and 10 C. striatus to burrow separately in individual 18.9-l buckets filled 22 cm deep with moistened, common test soil mixed from a clayey-loam collected on the grounds of the South Auburn University Fisheries Research Station. Adults were randomly selected for each bucket and placed in a centre thumb-depression, covered, and allowed to burrow. Excavated material consisted of amorphous piles rather than carefully constructed chimneys. After 48 h, species-specific excavations were shaped into similar, semi-circular mounds, keeping form and texture similar between crayfish species. Similar human-built mounds were constructed from the common test soil mixture that had no contact from test animals (Figure 2). We wore separate nitrile gloves for handling mounds and filling buckets to avoid cross-contamination of potential chemical cues.
Artificial burrow and mound layout in mesocosm experiments. Mesocosms were divided into sections (highlighted in white), each containing a treatment mound (C. diogenes, C. striatus, or human-built). Treatment mounds were arranged as similarly as possible. White markers indicate location of juveniles (burrowed or on surface) when cover removed.
Citation: Behaviour 154, 12 (2017) ; 10.1163/1568539X-00003463
Artificial burrow and mound layout in mesocosm experiments. Mesocosms were divided into sections (highlighted in white), each containing a treatment mound (C. diogenes, C. striatus, or human-built). Treatment mounds were arranged as similarly as possible. White markers indicate location of juveniles (burrowed or on surface) when cover removed.
Citation: Behaviour 154, 12 (2017) ; 10.1163/1568539X-00003463
Artificial burrow and mound layout in mesocosm experiments. Mesocosms were divided into sections (highlighted in white), each containing a treatment mound (C. diogenes, C. striatus, or human-built). Treatment mounds were arranged as similarly as possible. White markers indicate location of juveniles (burrowed or on surface) when cover removed.
Citation: Behaviour 154, 12 (2017) ; 10.1163/1568539X-00003463
We ran trials in ten 120-cm diameter (375 cm circumference, 11 309 cm2 total area) plastic-pool mesocosms, filled with 10.2 cm of test soil (not exposed to either species). Each mesocosm was divided into 3 equal sections (‘1’, ‘2’, or ‘3’) with a 1.25 cm diameter hole created 7.62 cm from the outside edge of each section (Figure 2) to represent an adult burrow. A C. diogenes mound, a similarly-sized C. striatus mound, and a human-built mound were randomly assigned a section in each mesocosm and placed around the corresponding ‘burrow’ hole. We assigned six randomly selected juveniles to each mesocosm, and placed them in the centre inside an inverted cup. After an hour acclimation, the cup was removed and mesocosms were covered to maintain dark, humid conditions. After 16 h, mesocosms were uncovered and we counted and marked the position of each juvenile using metal pins. Since some juveniles did not burrow, we marked both the total number of individuals and the total number of burrowed individuals and used these as separate and combined response variables. Two trials were run within 5 days with randomly selected animals (total mesocosm ). A generalized linear mixed model with Poisson error distribution was used to compare mean juvenile abundance and occupied burrow abundance among the three soil mound treatments. The model included treatment (C. diogenes, C. striatus, or human mound) as a fixed effect and mesocosm and run as random effects. To determine if there was an overall treatment effect, we used a likelihood ratio test to compare an intercept-only model (+ random effects) to a fixed effects model (+ random effects), which was followed with a post-hoc Tukey’s test if significant.
2.4. Experiment 3: grouping behaviour and site selection
To test whether juvenile C. diogenes exhibit grouping tendencies when selecting sites for burrowing, we allowed 6 juveniles to burrow in plastic pool mesocosms as above, except without adults or chimneys present (i.e., no adult or physical cues). For each trial, we added juveniles to the centre of the mesocosm and marked their distributions (total and burrowed) as above. All burrowed and non-burrowed individuals were marked as above and photographed with a Canon EOS Rebel T5 digital SLR camera. All images were captured perpendicular to the centre of the mesocosm at a fixed height (2 m) with a ruler added to the field of view for scale. Distances between each burrow were calculated in ImageJ software (Abramoff et al., 2004). From these calculated distances, nearest neighbor analysis (Clark & Evans, 1954) was performed to distinguish patterns of distribution. For each mesocosm, the mean observed nearest-neighbour distance () was divided by the expected mean distance under a random pattern of distribution (re, given by , density) to give R, a measure of departure from random. Distributions are random when , dispersed when and clumped when (Clark & Evans, 1954). Statistical significance for each trial was determined by standard Z scores. See Clark & Evans (1954) and Cade (1981) for calculation details. All analyses were performed in R (R Development Core Team, 2016).
3. Results
3.1. Experiment 1: effects of congeneric adults on site selection
All C. diogenes tested survived soil preference trials and burrowed within 48 h. All juveniles chose floodplain soils for burrowing. For ABCs containing a C. latimanus adult burrowing in streamside soil, 100% of C. diogenes juveniles selected the floodplain soils (, ). For ABCs containing a C. latimanus adult burrowing in floodplain soil, 100% of C. diogenes juveniles selected the floodplain soils (, ).
3.2. Experiment 2: effect of soil mound source on juvenile burrow location
In general, juvenile crayfishes tended to aggregate near soil mounds constructed by adult crayfish and avoid mounds constructed by humans. Of the 60 C. diogenes juveniles tested for burrow mound preference, 36 burrowed within the 16-h trial. Based on the likelihood ratio test, there was a significant overall treatment effect (, df = 2, ) on the total number of juveniles (burrowed + non-burrowed). Specifically, there was a significant effect in sections containing C. diogenes mounds (average number of juveniles ± SE = 2.9 ± 0.29, , ) but not in sections with C. striatus mounds (1.8 ± 0.36, , ) or human-built mounds (1.2 ± 0.12, , ). Tukey’s post hoc test revealed significantly more juveniles in C. diogenes sections than in human-built sections (, Figure 3). Of the 36 burrowed juveniles, there was also an overall significant treatment effect (, df = 2, ), with specific significant effects for the C. diogenes section (2.3 ± 0.26, , ) but not the C. striatus (0.8 ± 0.30, , ) or human-built (0.5 ± 0.18, , ) sections. Similarly, Tukey’s post hoc test revealed that there were significantly more juveniles burrowed in the C. diogenes section than in the human-built () and C. striatus () sections (Figure 3).
Mean number (+ SE) of juveniles per mesocosm section containing different chimney treatments. Top panel refer to all individuals (burrowed + surface), whereas bottom panel is mean number of juveniles that burrowed only. Letters above bars denote significant difference according to a post-hoc Tukey’s test.
Citation: Behaviour 154, 12 (2017) ; 10.1163/1568539X-00003463
Mean number (+ SE) of juveniles per mesocosm section containing different chimney treatments. Top panel refer to all individuals (burrowed + surface), whereas bottom panel is mean number of juveniles that burrowed only. Letters above bars denote significant difference according to a post-hoc Tukey’s test.
Citation: Behaviour 154, 12 (2017) ; 10.1163/1568539X-00003463
Mean number (+ SE) of juveniles per mesocosm section containing different chimney treatments. Top panel refer to all individuals (burrowed + surface), whereas bottom panel is mean number of juveniles that burrowed only. Letters above bars denote significant difference according to a post-hoc Tukey’s test.
Citation: Behaviour 154, 12 (2017) ; 10.1163/1568539X-00003463
3.3. Experiment 3: grouping behaviour and site selection
Of the 60 juveniles tested in the grouping trials, 9 were observed on the surface after 16 h. The number of burrowed crayfish in each mesocosm ranged from 3 to 6 (Table 1). In many instances, multiple crayfish occupied the same burrow, thus their nearest-neighbour distance was 0. Overall, observed mean nearest-neighbour distance ranged from 12.71 to 32.08 (Table 1), and R values for all trials were <1, indicating clumped distributions. Based on standard Z scores, 9 of the 10 trials were significant at , with the only trial not significantly clumped having a reduced number () of individuals burrowing (Table 1).
Nearest neighbour analysis for experiment 3 (group navigation).
4. Discussion
Navigation by animals to a target, such as suitable habitat, is influenced by a suite of environmental, idiothetic, and learned cues. To various degrees depending on the organism, these cues integrate multiple sensory processing systems (olfaction, chemosensory, vision, etc.) with the ultimate outcomes influenced by potential interactions and synergies between these systems (Knaden & Graham, 2016). Our experiments support earlier studies (Grow, 1982; Helms et al., 2013a) and suggest the importance of environmental cue integration, in this case soil substrate composition, conspecific adults, and group behaviour, for habitat selection and recruitment of juvenile burrowing crayfish.
Juvenile burrowing crayfish face a particular challenge when transitioning between aquatic and terrestrial environments. They must find suitable burrowing habitat while avoiding desiccation, predation, and other migratory risks. Accordingly, although burrowing + non-burrowing individuals showed strong differences between treatments, there were stronger species-specific effects of burrow-mound and group cues when we considered only the individuals that burrowed. We consider these burrowing individuals to be the individuals that ultimately would have survived desiccation and predation in a natural setting. However, suitable habitat is not the only consideration. Crayfish must burrow in close enough proximity to conspecifics if they are to find mates and successfully reproduce, which requires recognition and processing of a combination of cues associated with habitat and conspecifics. C. diogenes appear to be able to identify specific substrate types. They also appear to respond to cues provided from burrowed adults of the same species. In the absence of conspecifics, C. diogenes prefer fine (e.g., clay, silt) to coarse (e.g., sand) particle soils (Grow & Merchant, 1980). However, when adult conspecifics are present, juveniles burrow in close proximity to adults regardless of soil type (Helms et al., 2013a).
Several other crayfish species burrow in the same soil types as C. diogenes (Hobbs, 1981), thus one may expect juvenile C. diogenes to burrow in close proximity to congenerics if they were simply using the presence of crayfish burrows as an indicator of habitat suitability. However, in our study, using the same experimental apparatus as Helms et al. (2013a), juvenile C. diogenes consistently chose to burrow in fine, clayey soils regardless of the location of congeneric burrows. Together this suggests that attraction to conspecific burrows is driven by the integration of abiotic and species-specific biotic cues and that certain cues override others, as seen in the path integration and visual cues encountered by other species (e.g., Wehner et al., 1996). Further, since associating with conspecifics appears to trump burrowing in preferential soils, juvenile site selection in these crayfish may be more related to the benefits of intraspecific interactions like reproduction rather than habitat preference.
Species-specific detection has been demonstrated previously for crayfishes in aquatic environments where water is an effective medium for dispersal of chemical signals. Juvenile Orconectes sanbornii, O. virilis and Procambarus clarkii can discriminate between brooding and non-brooding individuals using chemical stimuli, with cues likely being species-specific (Little, 1975). Several species demonstrate conspecific, parent-offspring and/or kin recognition based on dispersed chemical cues (Dunham & Oh, 1992; Levi et al., 1999; Mathews, 2011). Chemical communication in general is prevalent in crayfish mating (Fero et al., 2007; Berry & Breithaupt, 2010), agonistic interactions (Breithaupt & Eger, 2002) and foraging (Wolf et al., 2004). Our results suggest that the cues used by C. diogenes can be detected in terrestrial, as well as aquatic environments; however, cue recognition among crayfish in terrestrial environments has received little attention, and how they navigate following a transition to terrestrial habitat is not well known. Wehner (1987) postulated that physical, physiological and behavioural components of a sensory system correspond to the environment carrying the most relevant signal (‘matched filters’). Multiple lines of evidence from this study and others (e.g., Keller et al., 2001) suggest that crayfish have such adaptations, but specifically how they differ in burrowing species is not well known.
The function of the soil mounds associated with crayfish burrows has been pondered for decades (Abbott, 1884). Several hypotheses exist as to why these are constructed, ranging from regulation of airflow (Hobbs, 1981), species recognition (Trepanier & Dunham, 1999; Punzalan et al., 2001), or simply discarded material from burrow enlargement (Walls & Layne, 2009). Our study supports the hypothesis that mounds function, at least in part, in species recognition. By associating burrow entrances with a constructed mound, the location of favourable habitat and presence of conspecifics is advertised. Previous studies show that crayfish mounds can attract conspecifics. Fallicambarus fodiens individuals are more likely to burrow near a conspecific-constructed chimney than a human-constructed one, and they prefer mud saturated with water exposed to a con-specific over mud saturated with distilled water (Punzalan et al., 2001). Further, F. fodiens and Orconectes rusticus have been shown to be capable of homing behaviours and that visual cues are unnecessary for success (Kamran & Moore, 2015). Our results confirm and extend these findings as we measured juvenile burrowing preference in an additional species (C. diogenes) and in association with 3 contrasting cue sources: human-built (tactile/visual cue only), congeneric (tactile/visual cue and general crayfish cue), and conspecific-constructed mounds (tactile/visual cue and species-specific cue). Juveniles navigated toward, and were more likely to burrow near, conspecific mounds over human-built and congeneric mounds, even when burrow complexes were unoccupied. This preference for burrowing near conspecific mounds, in the absence of conspecific occupants, suggests that site selection cues are species-specific and provided from the mound itself. Although not specifically tested for in this study, these cues are likely to be chemical, rather than visually or texturally based, as demonstrated for F. fodiens (Punzalan et al., 2001). During burrow enlargement and mound construction for C. diogenes, soil particles are formed meticulously into pellets with the third maxillipeds (Grow, 1981). These appendages are proximate to the nephropore, the excretory point of the green gland and source of many chemical cues associated with urine in crayfishes (Breithaupt, 2002). In our surface mesocosm study, experimental mounds were constructed such that width, height, and texture were standardized among treatments. If cues were entirely visual or tactile, we should have observed no preference for burrowing near conspecific mounds over human-built mounds, as both treatments were visually and texturally similar.
Crayfish are generally territorial with a propensity for agonistic, aggressive behaviours, thus showing low tolerance for other individuals (Gydemo et al., 1990; Figler et al., 1995; Fero & Moore, 2008). However, recent studies suggest that burrowing crayfish may be an exception as they show a level of conspecific tolerance usually not found in surface-dwelling species. High concentrations of individuals in burrowing habitats, the occupancy of single burrows by multiple individuals, and a lack of an escalated sequence of agonistic behaviours (Norrocky, 1991; Hamr & Richardson, 1994; Guiasu et al., 2005; Dalosto et al., 2013; Helms et al., 2013b) suggest a high level of conspecific tolerance. Similarly, we found juvenile C. diogenes to associate with both conspecific juveniles and adults. However, whether these observed associations reflect complex social structure or merely tolerance is unknown. It is likely that there is selective advantage to tolerating other individuals when exhibiting burrowing habits and burrowers may be released from the typical limiting resources experienced by open-water dwellers (Dalosto et al., 2013). Given the relatively specific environmental conditions required by burrowing crayfishes, such tolerance may be one of the mechanisms that have allowed them to persist in semi-terrestrial environments. However, burrows are a resource of high value and of considerable physiological cost to construct (Richardson, 2007), so increased agonistic interaction may be expected. Conclusive evidence of compelling reasons as to why burrowing species show increased tolerance and reduced agonist behaviour remain elusive.
Despite the territorial and agonistic behaviours typically observed in crayfishes, benefits of grouping are numerous. Quite often, organisms in groups can more effectively avoid predation (Hamilton, 1971), forage (Crook, 1960), consume less oxygen thus conserve energy (Ritz et al., 2001), and have increased mate accessibility (Dobson & Poole, 1998) over solitary individuals. Juvenile aggregation in particular has been observed in many invertebrate species (e.g., spiny lobsters, see Butler et al., 1999; Dolan & Butler, 2006; and porcelain crabs, see Jensen & Armstrong, 1991). This aggregation often coincides with optimal seasonal dispersal conditions suggesting timing is particularly important for vulnerable juveniles (Rasa & Anne, 1995; Palaoro et al., 2016). However, navigational error can be pervasive as a result of a limitation of cues, errors in interpretation and integration of cues, and environmental turbulence (Codling et al., 2007). Although it may seem like a daunting task for juvenile crayfish to emerge from aquatic habitats and traverse a forest floor to burrow, there is evidence that group movement can improve an individual’s ability to align and reach a target direction by the suppression of individual error by interactions and group cohesion (Simons, 2004). Further, aggregation is predicted to be more prevalent in turbulent or dangerous environments where the efficacy of navigational cues is limited (Simons, 2004). This ‘many-wrongs principle’ has been shown in migratory birds (Bergman & Donner, 1964), fish schooling in a turbulent environment (Grunbaum, 1998; Codling et al., 2007), and the foraging patterns of Bornean bearded pigs (Sus barbatus, Hancock et al., 2006). Whether this phenomenon explains our results is speculative; however, our observed patterns of aggregation suggest that there is some benefit to grouping, particularly for juveniles searching for potential burrowing sites. Although grouping was observed in our trials, some caution should be used in broad interpretation of our results, as juveniles used for grouping trials were reared from the same female. As such there could be a maternal imprint or some other brood-related influence on their behaviours. Further directed studies are needed to elucidate the true relationship between juvenile crayfish group size, relatedness and navigational success.
Our study sheds light on the burrowing site selection cues used by a common species of burrowing crayfish and provides insight on recruitment strategies used by burrowing crayfish in general. Our experiments suggest that juvenile C. diogenes integrate cues from the soil, locally burrowed adults, and each other for transitioning from semi-terrestrial habitats to preferred burrowing sites in the flood plain. Other studies have shown that burrowing crayfish have a stronger homing capability than non-burrowing crayfish (Kamran & Moore, 2015), although the mechanisms for this capacity remain elusive. Accumulating data suggest that burrowing crayfish are unique in that they have a semi-communal, shared-effort existence with a high tolerance of conspecifics, a strong chemosensory ability to detect volatile and water-soluble odour cues, and the ability to use these cues in conjunction with soil composition and juvenile aggregation to locate optimal burrowing habitat. Such traits may allow for continued recruitment in a heterogeneous environment.
Acknowledgements
Funding was provided by the National Science Foundation Research Experience for Undergraduates (REU) program. We thank Alan Wilson for directing and coordinating the warm-water aquatic ecology REU Site as well as Miriam Schmid, Adam Kelly, Michael Hart and Tom Hess for field and laboratory assistance. Also, we thank Jack Feminella, Sue Colvin, Stephen Sefick, Eric Bauer and Jenn Weber for constructive feedback on previous manuscript drafts. This is contribution No. 737 to the Auburn University Museum of Natural History.
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