A two‐step mechanism controls the timing of behaviour leading to emergence from soil in adult males of the scarab beetle Dasylepida ishigakiensis

Adults of the white grub beetle Dasylepida ishigakiensis Niijima et Kinoshita (Coleoptera: Scarabaeidae) emerge from the soil around dusk for mating on subtropical islands. The present study examines the factors controlling the emergence of males in the laboratory. There are two steps involved. Standby behaviour (i.e. insect head appears at the soil surface) can be observed for several hours before the beetles actually emerge for mating. The standby behaviour is facilitated by warm conditions, although the proportion of standby individuals is influenced not only by the temperature on that day, but also by that on the previous day. Experiments in which beetles are exposed to photoperiod and thermoperiod combinations, in and out of phase, show that temperature is more important in inducing standby and emerging behaviour than light alone. For the second step, factors such as temperature, light and the presence of the female sex pheromone determine whether males will leave the standby position and emerge onto the ground. The female sex pheromone stimulates standby beetles to exhibit emerging and wing vibration behaviours, although the effect depends on when it is presented to beetles. Beetles burrow back into the soil; this behaviour is influenced by illumination and time of the day but not by temperature. The results suggest that D. ishigakiensis possesses a sophisticated mechanism controlling male emergence from the soil.     

Observations of the migration of adult Dasylepida ishigakiensis (Coleoptera: Scarabaeidae) from belowground to the soil surface and their reproductive status by MRI

Field observations indicate that white grub beetles Dasylepida ishigakiensis Niijima et Kinoshita (Coleoptera: Scarabaeidae) pupate approximately 40 cm underground and then emerge from the soil surface as adults. Although the factors influencing adult emergence from the soil have been studied, the migration of adults from belowground to the surface has never been characterized. In this study, the vertical movement of virgin adults from natural eclosion depths to their emergence from the soil surface was investigated. Virgin adults were introduced at a depth of 40 cm from the soil surface in wooden-framed glass cases, and the vertical position of each individual was checked every day. Both females and males emerged near the soil surface at approximately day 50 after they were transferred from 24 °C to 18 °C conditions. The maturity of the ovaries in unemerged and emerged females was also observed by magnetic resonance imaging. All females that had emerged from the soil possessed developed oocytes, and most possessed mature eggs. The cross-sectional area of eggs was determined in magnetic resonance images and compared between unemerged and emerged females, and the egg areas of emerged females were significantly larger than those of unemerged females. Our results indicate that the timing of female emergence from soil corresponded to ovary maturity in this species.     

Extrinsic and Intrinsic Factors Influencing the Emerging and Burrowing Behaviors of Reproductively Active Adults of the White Grub Beetle, Dasylepida ishigakiensis

The subtropical scarab beetle, Dasylepida ishigakiensis, has a two-year life cycle. This study showed the time of adult emergence from the soil relative to the time of dusk and the presence of the female sex pheromone. Beetles collected on Miyako Island were transported to Tsukuba where they were immediately placed under natural day lengths in February. They exhibited two emergence peaks that corresponded to the times of dusk in Tsukuba and on the island, respectively. Males emerged precociously if a lure containing synthetic female sex pheromone was placed in their container, whereas the females’ behavior was unaffected. Previous observations that mated females dig deeper in the soil than virgin females, males or mated males were confirmed. To explore the underlying mechanism controlling the behavioral change associated with mating, liquid material derived from the male accessory glands, seminal vesicles and female bursa copulatrix was injected into beetles, but without any significant influence on burrowing behavior. No significant influence was also observed in beetles injected with anisomycin, an inhibitor of protein synthesis related to memory in other animals.     

Crepuscular activity of adult Sericesthis geminata (Coleoptera: Scarabaeidae): Influence of circadian rhythmicity and light intensity

Subterranean Sericesthis geminata (Boisduval) beetles emerge from the soil daily during the flight season. Emergence and flight are initiated within 15 min after sunset. The beetles are active above the soil surface as the intensity of illumination decreases from 240 lux to 0.7 lux.

If young adult beetles still in their pupal cells in the soil are placed under constant, low‐intensity illumination, they first emerge at any time of day, showing no cyclical diurnal activity pattern. When such beetles are exposed to diurnal fluctuations in illuminance, the first emergence and flight occur at dusk. These beetles subsequently show a diurnal rhythm in their activity, even when exposed to constant environmental conditions. This endogenous activity cycle has a period of about 22 h, and is synchronised with diurnal fluctuations in light intensity. It is reset in response to a change in the photoperiod.

The data suggest that, after initial emergence from the soil, daily crepuscular activity is initiated by an endogenously controlled activity rhythm which causes the beetles to burrow to the soil surface shortly before dusk. At the soil surface they are exposed to fluctuations in the duration and intensity of illumination which may reset the endogenous rhythm, affecting the time of subsequent emergence.     

A versatile laboratory stream with examples of its use in the investigation of invertebrate behaviour

A versatile and simple laboratory stream was designed and used to investigate the burrowing activity of two insects in response to changes in water velocity and substrate type.Aphelocheirus aestivalis adults were unable to burrow into sand, however, a small proportion of juveniles did burrow in this substrate. The presence of sand in gravel reduced the burrowing success of adults. Steady increases in flow stimulated the burrowing response of both adults and juveniles on gravel and sandy gravel.Ephemera danica was unable to burrow in sand alone at the velocities used in the experiment. The presence of particles greater than 2 mm in diameter in the substrate appeared to be essential for successful burrowing under the test conditions. An increase in flow from 3 to 8 cm s^–1 resulted in an increase in burrowing. The time taken for each specimen to burrow varied widely within replicate tests but most specimens had penetrated the substrate within 150 seconds of introduction. The implications of these observations in influencing the microdistribution of these species are discussed.     

Breeding Strategies in Females of the Parasitoid Wasp Spalangia endius: Effects of Mating Status and Size

Does the mating status or body size of a female parasitoid wasp affect her host size choice or propensity to burrow? In Spalangia endius, using smaller hosts appears to reduce a female's cost of parasitization but not her son's fitness. However, virgin females, which produce only sons, did not preferentially parasitize smaller hosts. Mated females also showed no host size preference. Mated females burrowed more than virgins in the presence of hosts, although not in their absence. Burrowing may reduce a mated female's harassment from males, and not burrowing may increase a virgin female's chance of mating because males avoid burrowing. Mating did not increase female longevity. Greater female size increased the offspring production of mated females burrowing for hosts but not in the absence of burrowing and not in virgin females. A female's size had no significant effect on whether her first drill attempt was on a large or a small host or on the duration of her successful drills.     

Burrow architecture and digging activity in the Cape dune mole rat

While females are traditionally thought to invest more time and energy into parental care than males, males often invest more resources into searching and displaying for mates, obtaining mates and in male–male conflict. Solitary subterranean mammals perform these activities in a particularly challenging niche, necessitating energetically expensive burrowing to both search for mates and forage for food. This restriction presumably affects males more than females as the former are thought to dig longer tunnels that cover greater distances to search for females. We excavated burrow systems of male and female Cape dune mole rats Bathyergus suillus the, largest truly subterranean mammal, to investigate whether male burrows differ from those of females in ways that reflect mate searching by males. We consider burrow architecture (length, internal dimensions, fractal dimension of tunnel systems, number of nesting chambers and mole mounds on the surface) in relation to mating strategy. Males excavated significantly longer burrow systems with higher fractal dimensions and larger burrow areas than females. Male burrow systems were also significantly farther from one another than females were from other females' burrow systems. However, no sex differences were evident in tunnel cross-sectional area, mass of soil excavated per mound, number of mounds produced per unit burrow length or mass of soil excavated per burrow system. Hence, while males may use their habitat differently from females, they do not appear to differ in the dimensions of the tunnels they create. Thus, exploration and use of the habitat differs between the sexes, which may be a consequence of sex differences in mating behaviour and greater demands for food.     

Postnatal development of subterranean habits in tuco-tucos <Emphasis Type="Italic">Ctenomys talarum</Emphasis> (Rodentia,Caviomorpha, Ctenomyidae)

Postnatal development of subterranean habits was investigated in Los Talas’ tuco-tuco Ctenomys talarum, a subterranean caviomorph rodent endemic from South America. Since in this species, some key morpho-functional traits related to scratch-digging behaviour—a form of underground progression—are already present during early ontogeny and develop progressively, we predicted that this behaviour expresses early during postanatal development and its performance enhances gradually from pups to adults. The process of acquisition of different behaviours associated to the construction of a burrow system was recorded in 11 individuals, each one coming from different litters, inside a terrarium filled with natural soil. We found that scratch-digging and burrowing behaviours expressed early during postnatal development, particularly, during lactancy. The digging of a “true burrow” clearly preceded the dispersal age, with a high inter-individual variability, from 18 (lactancy) to 47 (post-weaning) postnatal days. Pups could lose the soil using their foreclaws and remove the accumulated substrate using their hindfeet as adults do. During lactancy individuals could construct a simple burrow to shelter, and first burrow construction occurred in the absence of either a burrowing demonstrator or an early subterranean environment (a natal burrow). However, certain features of the complex burrow system that characterize this species, such as lateral branches and nest chamber, just appeared after weaning. The time elapsed until animals started to dig and the time dedicated to underground activities varied with age, decreasing and increasing, respectively. In sum, our results show that—in C. talarum—immature digging behaviour gets expressed early during ontogeny, and develops progressively. The role of the early ability to build its own burrow and its possible function influencing the development of musculoskeletal traits and on efficiency for such conduct is discussed.     

Familiarity and flexible mating strategies of a solitary rodent, Dipodomys ingens

Because mating is a product of individual reproductive strategies that may vary with changing conditions, we predicted variable mating behaviour in an arid-adapted, territorial rodent, the giant kangaroo rat, Dipodomys ingens. We also predicted that familiarity would facilitate nonaggressive courtship and mating in this solitary rodent. Through direct observations in the field, we found that mating varied from exclusive to multiple partners. Where densities were low, and on nights when multiple females were in oestrus, each animal mated with one member of the opposite sex. In conditions where the operational sex ratio was skewed towards multiple males, males footdrummed and competed for females. Males were able to mate with one or two females in adjacent territories, and they successfully competed for these same females throughout the breeding season. Females that mated exclusively with one male had more pups emerge from the burrow compared with females that experienced male competition. Females allowed nearest neighbour males to enter their burrows, and they engaged in more nonaggressive contact with close neighbours than with other males. Paired encounters in the field showed less aggression towards neighbours than strangers. In laboratory tests, females were less aggressive towards and allowed more contact with familiar than unfamiliar males. These results show that D. ingens can alter mating strategies as conditions change. Familiarity is an important factor in nonaggressive interactions between males and females and may be important to mate preferences in females during reproduction. The less aggressive behaviour to neighbours than to strangers (‘dear enemy’ phenomenon) is consistent with other solitary animals that defend multipurpose territories. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

How Old are Colonizing Hypothenemus hampei (Ferrari) Females When They Leave the Native Coffee Fruit?

The age of colonizing Hypothenemus hampei (Ferrari) females when they leave the native coffee fruit was determined under laboratory conditions. This biological parameter might be useful for planning experiments with this species because certain physiological statuses are expressed from or until a determined age, which in turn may determine the response of individuals to different treatments. An experimental device was used to simulate the conditions inside a coffee berry and to permit the observation of the abandonment behavior of the beetles. Virgin and mated females with or without melanized cuticles were used in the experiments. On average, colonizing coffee berry borers were 15-days-old at the moment of host abandonment. Females at this age were mated, had full dark cuticles, and were able to display flight and lay viable eggs. Interestingly, H. hampei females that mated before they acquire a fully dark cuticle abandoned the host 1.7 times faster than females that mated after they reach this physiological status. Further studies into food conditions and their impacts on the pre- abandonment of H. hampei females are encouraged.     

Rhythmic egg-laying behaviour in virgin females of fruit flies Drosophila melanogaster

Fruit fly Drosophila melanogaster females display rhythmic egg-laying under 12:12?h light/dark (LD) cycles which persists with near 24?h periodicity under constant darkness (DD). We have shown previously that persistence of this rhythm does not require the neurons expressing pigment dispersing factor (PDF), thought to be the canonical circadian pacemakers, and proposed that it could be controlled by peripheral clocks or regulated/triggered by the act of mating. We assayed egg-laying behaviour of wild-type Canton S (CS) females under LD, DD and constant light (LL) conditions in three different physiological states; as virgins, as females allowed to mate with males for 1?day and as females allowed to mate for the entire duration of the assay. Here, we report the presence of a circadian rhythm in egg-laying in virgin D. melanogaster females. We also found that egg-laying behaviour of 70 and 90% females from all the three male presence/absence protocols follows circadian rhythmicity under DD and LL, with periods ranging between 18 and 30?h. The egg-laying rhythm of all virgin females synchronized to LD cycles with a peak occurring soon after lights-off. The rhythm in virgins was remarkably robust with maximum number of eggs deposited immediately after lights-off in contrast to mated females which show higher egg-laying during the day. These results suggest that the egg-laying rhythm of D. melanogaster is endogenously driven and is neither regulated nor triggered by the act of mating; instead, the presence of males results in reduction in entrainment to LD cycles.     

Burrow behaviour,structure and utilization of the amphibious mudskipper Periophthalmus chrysospilos Bleeker, 1853 in the Mekong Delta

Burrows of fishes are important to their creators, but knowledge of burrowing behaviour, structure and utilization are poorly understood. We report the burrowing behaviour of the amphibious mudskipper, Periophthalmus chysospilos, from estuarine and coastal sites within the Mekong Delta (Vietnam). Activities at and around the burrow were observed over 12 months (April 2020 to March 2021). Burrow casts were recovered monthly to determine burrow structure and utilization in this species. Observations revealed that males excavate burrows with their mouths during the ebb tide. Burrows were J-, Y- and U-shaped, with 1–2 openings to the surface and a bulbous egg chamber. The burrow depth (BD) and total length (BL) varied with shape and site, but not season. The BD and BL ranged from 15.1 ± 0.9 to 18.6 ± 0.80 SE cm and from 22.1 ± 1.2 to 25.7 ± 1.0 SE (standard error of mean) cm, respectively. These results provide insights into the burrowing ability and better understand the ecology of these fishes in the Mekong Delta.Running head: Burrow behaviour, structure and utilization of Periophthalmus chrysospilos.     

Mating alters the link between movement activity and pattern in the red flour beetle

Mating in arthropods is costly and has negative effects on survival. Such effects are often more strongly expressed when individuals are simultaneously exposed to other stress sources. Consequently, the behaviour of virgin and mated individuals often differs. Mated females, for example, search for suitable oviposition sites, whereas virgin females search more for mates. In the present study, we examine the effect of mating separately for females and males on four key behaviours of the red flour beetles: movement activity, movement along the edges of an arena, latency to emerge from shelter and preference for dark microhabitat. After mating, both sexes increase their activity at the same time as moving less along the arena edge, leading to a change in movement pattern. Females possibly change their movement pattern to locate suitable oviposition sites, whereas males perhaps do so to detect additional females with which to mate. Latency to emerge from shelter and dark preference are not influenced by mating, although they increase when measured again after 1 week. Of these behaviours, only movement activity is consistent at the individual level. We also examine whether mating incurs a cost as expressed in the time required to recover from a chill‐coma. The latter is a common proxy of cold tolerance in ectotherms. By contrast to our prediction, mating has no effect on chill‐coma recovery time, suggesting that either a single mating event does not incur sufficient stress or that there is possibly no trade‐off between the energetic cost of mating and of cold tolerance.     

Paternal effort and its relation to mating success in the European ground squirrel

The necessity for parental care is a driving force for determining mating systems and social organization. The European ground squirrel, Spermophilus citellus, is a polygynous, gregarious species in which male parental behaviour would not be expected. We had observed males digging in litter burrows that were later occupied by females and their offspring. Males never stayed overnight within these burrows. To determine whether this was some kind of paternal effort we tested the following hypotheses: (1) that male burrowing behaviour was directed towards the male's own offspring or towards the pregnant or lactating mother of the male's offspring; (2) that this behaviour had costs in terms of condition, decreased survival or fecundity; and (3) that it benefited offspring condition or survival. All three assumptions were met. Males worked on the litter burrow of their copulatory partners. Thus, this behaviour was directed towards the male's potential offspring. Male burrowing costs were seen in decreased foraging time and increased body mass loss. Offspring benefits were evident in increased mass at natal emergence. We conclude that male digging at litter burrows can be considered as paternal effort. Lastly, we considered the effects of polygyny on this male parental effort by comparing mating effort, mating success and paternal effort. High mating success was associated with high mating effort and low paternal effort. Moderate to low mating success was associated with lower mating effort and higher paternal effort, indicating a trade-off between the two.     

Reproductive effort during gestation and lactation by Richardson's ground squirrels

Summary Reproductive effort by yearling and older female Richardson's ground squirrels was studied over a 4-year period in southern Alberta by obtaining serial weight records from marked individuals to compare the mother's mass at critical points in the annual cycle (emergence from hibernation, estrus, parturition, and litter emergence) with her litter's mass at birth and weaning. Yearlings weighed only 80% of older adults at emergence from hibernation, but they mated at the same time as older females, attained adult mass coincident with pregnancy, and weaned litters that were not significantly smaller in size or mass than those of older females. Age and maternal mass were weak predictors of litter size and litter mass. Of the net increase in mass of the combined mother-litter unit during gestation, over half (60% of 139 g for yearlings; 52% of 127 g for older females) was attributable to an increase in the mother's own mass, whereas during lactation almost all of the net increase (93% of 545 g for yearlings; 96% of 567 g for older females) was attributable to an increase in the litter's mass. On a daily basis, deposition of mass in the litter was 6 times greater during lactation than gestation. On average, neonates weighed 2.3% (6.5 g) of maternal mass at birth and 23.1% (81 g) at emergence from the natal burrow; offspring masses at birth and at emergence were significantly negatively correlated with litter size. On average, litters weighed 16.3% (48 g) of maternal mass at birth and 157.5% (578 g) at emergence from the natal burrow. Compared with other hibernating sciurids, Richardson's ground squirrels have a similar offspring mass relative to maternal mass both at birth and at emergence from the natal burrow. However, because of the large litter size (typically 6–8), absolute reproductive effort, measured either as litter mass at birth or at natal emergence, is large for the body size of the species.     

The ecological significance of burrowing behaviour in the toad (Bufo viridis)

Summary The burrowing behaviour of the toad Bufo viridis was studied in the laboratory on soil containing 11–13% moisture. These toads usually excavate shallow, temporary burrows from which they emerge intermittently. Time spent subsurface increases with rising ambient temperature in the range of 18–30° C. In these conditions, water loss is effectively reduced and a new water balance is achieved. On return to water access, after two months on soil, the toads rapidly regain only that amount of water lost previously. It is concluded that this temperature-sensitive burrowing behaviour is an important factor in these animals' successful survival in semi-arid conditions.     

Rythme d'activité endogène chez un nébaliacé (Crustace phyllocaride)

In constant conditions and continuous darkness, the burrowing species Nebalia bipes (Fabricius) exhibits a clear circadian rhythm of emergence from the substratum and of swimming activity. The rhythm, in which activity occurs during the ‘expected night’, is obvious in both males and females and can remain overt for several weeks.The ‘free-running period’, although variable, is ≈ 24 h 20 min in a calm environment and at 18 °C. During the first day of the experiments, the swimming activity of freshly collected animals increases abruptly at dusk and then decreases gradually towards dawn. It has been possible to change the phase of the rhythm by subjecting the animals to a reversed LD schedule.The synchronization seems to result from the high photonegativity of Nebalia in normal daylight. The results of some experiments carried out with young juvenile animals suggests that the synchronization may possibly take place during the incubation period.     

Burrow structure and foraging costs in the fossorial rodent,Thomomys bottae

Summary A model for calculating the energy cost of burrowing by fossorial rodents is presented and used to examine the energetics of foraging by burrowing. The pocket gopher Thomomys bottae (Rodentia: Geomyidae) digs burrows for access to food. Feeding tunnels of Thomomys are broken into segments by laterals to the surface that are used to dispose of excavated soil. Energy cost of burrowing depends on both soil type and on burrow structure, defined by the length of burrow segments, angle of ascent of laterals, depth of feeding tunnels, and burrow diameter. In a desert scrub habitat, Thomomys adjust burrow segment length to minimize cost of burrowing. Observed segment lengths (mean=1.33 m) closely approximate the minimum-cost segment length of 1.22 m. Minimizing energy expended per meter of tunnel constructed maximizes efficiency of foraging by burrowing in the desert scrub. Burrow diameter and cost of burrowing increase with body size, while benefits do not, so foraging by burrowing becomes less enconomical as body size increases. Maximum possible body size of fossorial mammals depends on habitat productivity and energy cost of burrowing in local soils.     

Substrate selection by Carabus clatratus (Coleoptera, Carabidae) and its consequences for offspring development

In insects, habitat selection should be most distinctly effected by females during oviposition, and this choice should directly affect the performance of the less mobile offspring stages. To date, this behaviour has been poorly investigated in carabid beetles. This study examines sexual differences in microhabitat selection as well as egg-laying behaviour and its consequences for offspring in the stenoecious beetle Carabus clatratus. Laboratory experiments with adults and different offspring stages were undertaken to test the impact of soil moisture and substrate type on microhabitat selection and immature fitness. Only females changed their substrate selection behaviour after copulation, revealing a distinct preference for wet peat for oviposition. Egg mortality was less than 7% under both wet and dry soil conditions. In contrast to other investigations, egg mortality in C. clatratus was therefore of minor importance. Larval mortality was also low, but mortality of third-instar larvae and the pupal stage increased strongly under dry conditions. Furthermore, beetles that developed under dry conditions showed a significantly higher proportion of exoskeleton deformations, and immature adults were smaller when reared under low moisture conditions. The importance of a strong oviposition site selection for wet peat to ensure sufficient moisture conditions for offspring in the stenoecious species C. clatratus is discussed. Received: 14 December 1998 / Accepted: 15 July 1999     

Small males emerge earlier than large males in Dawson's burrowing bee (Amegilla dawsoni) (Hymenoptera: Anthophorini)

Females of Dawson's burrowing bee ( Amegilla dawsoni ) are receptive to the males as they emerge but have become unreceptive by the time they begin to nest. In addition, there is a single emergence period per year lasting about a month. These factors are predicted to lead to protandry and males of Dawson's burrowing bee do tend to emerge earlier in the annual flight season than females. Moreover, even during a single day, emerging males tend to precede females. The degree of protandry, however, is size-dependent, with smaller males tending to precede larger ones, both over the course of the flight season and on any given day. Because small males are at a disadvantage in the fights that occur for females, the earlier emergence of minor males may be a sexually selected response that reduces the likelihood that they will be displaced from potential mates by larger rivals.