Dopaminergic system as the mechanism underlying personality in a beetle

Individuals in many animal species exhibit 'personality,' consistent differences in behaviour across time, situations and/or contexts. Previous work has revealed a negative genetic correlation between intensity of tonic immobility and walking activity levels in the confused flour beetle, Tribolium confusum, thus suggesting these beetles exhibit personality in activity-related traits. The present study investigated the mechanism underlying this correlation. We used individuals derived from two strains established via artificial divergent selection for duration of tonic immobility. "Long" (L) strains exhibited higher frequencies and longer durations of tonic immobility, and lower activity levels, while "Short" (S) strains exhibited lower frequencies and shorter durations of tonic immobility and higher activity levels. We found that the duration of tonic immobility, and activity level, could be altered by caffeine administration; L strains fed with caffeine exhibited decreased durations of tonic immobility and increased activity levels. We also found that brain dopamine levels were lower in L strains than in S strains. Consequently, this study demonstrates that the dopaminergic system plays an important part in controlling the genetic correlation between tonic immobility and activity levels in this species.     

Biogenic amines, caffeine and tonic immobility in Tribolium castaneum

Biogenic amines are physiologically neuroactive substances that affect behavioural and physiological traits in invertebrates. In the present study, the effects of dopamine, octopamine, tyramine and serotonin on tonic immobility, or death-feigning, were investigated in Tribolium castaneum. These amines were injected into the abdomens of beetles artificially selected for long or short duration of tonic immobility. In beetles of the long strains, the durations of tonic immobility were shortened by injection of dopamine, octopamine and tyramine, and the effects of these amines were dose-dependent. On the other hand, serotonin injection did not affect the duration of tonic immobility. In the short-strain beetles that rarely feign death, no significant effects of the amines were found on the duration of tonic immobility. Brain expression levels of octopamine, tyramine and serotonin did not differ between long- and short-strain beetles, in contrast to the higher dopamine levels in short strains previously reported. Caffeine decreased the duration of death-feigning in both oral absorption and injection experiments. It is known that caffeine activates dopamine. Therefore, the present results suggest that the duration of tonic immobility is affected by dopamine via the dopamine receptor in T. castaneum.     

Forelimb dimensions and goniometry of the wrist and fingers in tufted capuchin monkeys (Cebus apella): Developmental and comparative aspects

Adult capuchin monkeys use precision grips during manipulation of small objects, although their thumbs have been classified as pseudo-opposable. We investigated the physical properties of the hands to increase our understanding of manual function in capuchins. Forelimb dimensions and joint mobility (goniometric) measurements were obtained from adult, juvenile, and infant tufted capuchins (Cebus apella). Compared to adult squirrel monkeys, adult capuchins exhibited less flexibility of the wrist and digits. Capuchins of all ages had proportionally longer hands than squirrel monkeys, and capuchins more than 7 weeks old had proportionally longer thumbs than squirrel monkeys. Growth of the arms and hands was asynchronous. The duration of growth of the thumb was particularly prolonged, extending into early adulthood. Age-related changes in flexibility were apparent in most indices, and were greatest at the metacarpophalangeal joints. It is unknown to what extent the characteristics of growth, forelimb dimensions, and goniometry presented by capuchins are shared with other species, or if they contribute to the capuchin's unusual prehensive capacities. However, the marked differences between adult capuchins and squirrel monkeys in these metrics, and between capuchins and rhesus in the growth patterns of the digits, suggest that variation across taxa in these characteristics can be considerable.     

Factorial correspondence analysis of fear-related behaviour traits in Japanese quail

Factorial correspondence analysis was performed on 341 quails from a F2 cross between two lines divergently selected on the duration of tonic immobility over 29 generations. Several fear- or stress-related traits were recorded, i.e. tonic immobility duration, number of inductions needed to induce tonic immobility, open-field behaviour (time spent walking, latency before first movement and number of defecations), asymmetry of tibia lengths and corticosterone concentration after restraint stress. Variables were categorised in classes and analysed by factorial correspondence analysis. The first axis was mostly described by open-field behaviour, and the second by tonic immobility traits (duration of tonic immobility and number of inductions), which showed that these behaviours were almost independent. No relationship was found between axes of the factorial correspondence analysis and corticosterone concentration or asymmetry of tibia lengths, showing that these variables reflected other characteristics of stress susceptibility than those described by tonic immobility and open-field behaviour. These results show that reaction to stress of quails is a multidimensional trait and cannot be summarised by one trait.     

Association between vent pecking and fluctuating asymmetry, heterophil to lymphocyte ratio, and tonic immobility duration in chickens

The purpose of the present study was to analyze the relationship between incidence of vent pecking, fluctuating asymmetry, heterophil to lymphocyte ratio, and tonic immobility duration in chickens. The experiment (140 birds in three different replicates) measured the fluctuating asymmetry of several traits (middle toe length, leg length, wing length, wattle length, and leg width), the heterophil to lymphocyte ratio, and the tonic immobility duration in 20-week-old pullets of five Spanish breeds of chickens (Blue Andaluza, Quail Castellana, White-faced Spanish, Red-barred Vasca, and Birchen Leonesa), and a White Leghorn population, with and without evidence of suffering from vent pecking. The number of birds per breed was 20, 24, 12, 20, 18, and 46, respectively. There was a significant difference between vent pecked and non-vent pecked birds on the relative fluctuating asymmetry of middle toe length (P < 0.05), the relative fluctuating asymmetry of birds who suffered from vent pecking being larger. The combined relative fluctuating asymmetry of the five traits approached levels of statistical significance (P = 0.08). There was a significant difference (P < 0.001) in heterophil to lymphocyte ratio and tonic immobility duration between vent pecked and non-vent pecked birds, the ratio being higher and the duration being longer in the group of birds that suffered from vent pecking. Thus, vent pecked birds were more asymmetrical, stressed and fearful than non-vent pecked birds, having increased relative fluctuating asymmetry, heterophil to lymphocyte ratio and tonic immobility duration. Differences were consistent across the breeds. Results indicate that vent pecking is associated with other measures of stress e.g. fluctuating asymmetry, heterophil to lymphocyte ratio, and tonic immobility duration.     

ON THE MECHANISM OF TONIC IMMOBILITY IN VERTEBRATES

1. The durations of successive periods of induced tonic immobility in the lizard Anolis carolinensis was examined as a function of temperature. An automatic recording method was employed and observations were made of 12,000 to 15,000 immobilizations with six animals over a temperature range of 5° to 35°C. during 5 months. 2. The durations of the immobile periods were found to vary rhythmically in most cases. The reciprocal of the duration of the rhythm, i.e., the rate of change of the process underlying the rhythms, when plotted as a function of temperature according to the Arrhenius equation show distributions of points in two straight line groups. One of these groups or bands of points extends throughout the entire temperature range with a temperature characteristic of approximately µ = 31,000 calories, and the other covers the range of 20° to 35°C. with µ equal to approximately 9,000 calories. 3. The initial stimulus in a series of inductions of immobility appears to set off a mechanism which determines the duration of the state of quiescence. Succeeding forced recoveries seem to have no effect on the normal duration of the rhythm. 4. These results are interpreted by assuming the release, through reflex stimulation, of hormonal substances, one effective between 5° and 35°C. and the other effective between 20° and 35°C. These substances are assumed to act as selective inhibitors of impulses from so called "higher centers," allowing impulses from tonic centers to pass to the muscles. 5. In some experiments a progressive lengthening in successively induced periods of immobility was observed. The logarithm of the frequency of recovery when plotted against time in most of these cases (i.e., except for a few in which irregularities occurred) gave a linear function of negative slope which was substantially unaffected by temperature. In these cases it is assumed that a diffusion process is controlling the amount of available A substance. 6. The results are similar to those obtained by Crozier with Cylisticus convexus. The duration of tonic immobility seems to be maintained in both arthropod and vertebrate by the chemical activity of "hormonal" selective inhibitors. The details of the mechanisms differ, but there is basic similarity. 7. Injections of small amounts of adrenalin above a threshold value are found to prolong the durations of tonic immobility of Anolis, by an amount which is a logarithmic function of the "dose." It is possible that internally secreted adrenalin, above a threshold amount, may be involved in the maintenance of tonic immobility. 8. The production of tonic immobility reflexly is a problem distinct from that of the duration of immobility. It is suggested that the onset may be induced by "shock" to the centers of reflex tonus causing promiscuous discharge of these centers with accompanying inhibition of the higher centers. Such a condition may result when an animal is suddenly lifted from the substratum and overturned, or when, as in the case of Anolis, it struggles with dorsum down. This reaction of the "tonic centers" may at the same time lead to discharge of the adrenal glands by way of their spinal connections thus prolonging the state.     

Selection for tonic immobility duration does not affect the response to novelty in quail

Genetic selection on a single fear test, the tonic immobility test, seems to result in selection on fearfulness, i.e. the propensity to exhibit fear responses, whatever the fear tests used. However, the conception of fear as a single variable has been challenged by the recognition that fear is multidimensional. This study was designed to test whether genetic selection on a classic index of fear in birds, tonic immobility duration, is accompanied by changes in the response to a single dimension of fear – novelty.Two lines of quail divergently selected for long (LTI) or short (STI) duration of tonic immobility were exposed to a novel object in their home cage. Quail of both lines showed typical fear reactions in response to novelty but there was no difference between lines. We conclude that genetic selection for tonic immobility duration does not affect all dimensions of fear, notably not novelty. Further studies are needed to investigate the dimensions of fear on which the two lines of quail could have been selected.     

Response to novelty inSaimiri andCallicebus: Influence of social context

Responses to novel objects by pair-livingSaimiri andCallicebus and grouplivingSaimiri were investigated in two experiments. In the first, titis and squirrel monkeys were tested in the presence and absence of an opposite-sexed pairmate. The species were differentially affected by the absence of the pairmate: titis of both sexes were distressed and object interest was attenuated; squirrel monkeys were not distressed and object scores (particularly females') increased. Nonsocial differences in object exploration principally involved the tempo and mode of investigation; squirrel monkeys were quicker and more vigorous than titis. In the second experiment, presence of a novel object was found to attract and arouse grouplivingSaimiri, as indicated by the change in the frequency and nature of social interactions and spatial distribution. Within- and between-sex social interactions reflected the typical female nucleus-peripheral male pattern seen inSaimiri groups in other environments. Species differences in investigatory patterns were considered to be contributing elements in the maintenance of distinctive life-styles.     

Prenatal growth of long bones in rhesus and squirrel monkeys (Macaca mulatta and Saimiri sciureus)

Fetal long bone growth was studied from 59 radiographs representing 35 macaques and 79 radiographs representing 16 squirrel monkeys. From lateral abdominal radiographs of pregnant females total lengths of long bone shadows were measured to the nearest millimeter with a sliding caliper. A linear regression line was fitted to the data for each species. The high correlation coefficients (min. = 0.92) indicated not only that over 80% of the variance in longbone length was associated with the regression but also that linear regression was an acceptable model. It was determined that the macaque long bones grew more rapidly prenatally than the squirrel monkey long bones. Saimiri long bones grew at a faster rate during the second half of gestation than would be expected considering that the macaque long bones were approximately twice the length of Saimiri long bones at birth and that the duration of their gestation was about the same. Thus squirrel monkeys must achieve a greater percentage of their birth size during the second half of gestation.     

Studies of heart disease and failure in aged female squirrel monkeys (Saimiri sp.)

Lesions consistent with heart failure were found in 23 of 88 adult squirrel monkeys that died between 1995 and 1999 at the Squirrel Monkey Breeding and Research Resource (SMBRR). This provided a rationale for a study surveying aged animals in the SMBRR for normal cardiac characteristics, using echocardiography (ECHO) and electro-cardiogram. In the pilot study, ECHO and electrocardiography were performed on 59 healthy female squirrel monkeys aged 10 years or older and 39 five-year-old monkeys. Parameters were heart rate, P-wave duration and amplitude, and PR, QRS, and QT intervals (electrocardiography), and ejection fraction. Two animals with cardiomyopathy were identified and received similar testing. Advanced-study animals had the same measurements, plus left ventricular internal diameter-systole (LVIDs) and -diastole (LVIDd), left atrial diameter-diastole (LADd) and aortic root diameter-diastole (AoRDd) by use of ECHO. Significant differences were found between groups in LADd, and P-wave and QRS interval durations. In a clinical context, these differences were not considered to be substantial. Normal aged female squirrel monkeys had significant increases in heart dimension and longer P- and QRS-wave durations than did monkeys of a five-year-old control group, although the increases were not considered clinically relevant. This study documents myocardial dynamics in healthy saimiri and those with cardiomyopathy.     

Sex and strain comparisons of tonic immobility (“Righting time”) in the domestic fowl and the effects of various methods of induction

Tonic immobility was induced in adult laying hens using different methods and substrates, factors which have shown great variety of response in previous work. The fact that topic immobility was induced in every situation confirms the robust nature of this phenomenon. Placing hens on their backs and restraining them in a U-shaped wooden cradle covered with cloth was the most reliable and consistent method. Not only was the duration of response greatest when this method was used, but less handling, with its possible stressful effects, was required to induce it. There were no significant differences in the latency to the first head movement or in the duration of immobility between adolescent ‘T’ (Rhode Island Red × Light Sussex) and ‘S’ (White Leghorn) lines but both these characteristics were considerably shorter in the ‘J’ line birds (Brown Leghorn). There were no significant sex differences in the duration of tonic immobility but male ‘T’ and ‘S’ line birds showed greater latencies to the first head movement and fewer subsequent alert head movements than females. These results are discussed in terms of sex and strain differences in fearfulness.The varied nomenclature used to describe the immobility reaction is discussed and an alternative term “righting time” is proposed. It is further suggested that the immobility response consists of an inhibitory and an alert stage.     

Gustatory responsiveness to monosodium glutamate and sodium chloride in four species of nonhuman primates

The taste responsiveness of six squirrel monkeys, five pigtail macaques, four olive baboons and four spider monkeys to monsodium glutamate (MSG) and to sodium chloride was assessed in two-bottle preference tests of brief duration (2 min). When given the choice between tap water and defined concentrations of the two tastants dissolved in tap water, the animals were found to significantly discriminate concentrations of MSG as low as 2 mM (spider monkeys and olive baboons), 50 mM (pigtail macaques) and 300 mM (squirrel monkeys) from the solvent. With sodium chloride, taste preference thresholds were found to be 1 mM (spider monkeys), 20 mM (pigtail macaques), 50 mM (olive baboons), and 200 mM (squirrel monkeys), respectively. Across-species comparisons of the degree of preference for MSG and sodium chloride displayed by the four primate species showed the same order of spider monkeys>olive baboons>pigtail macaques>squirrel monkeys. When presented with equimolar concentrations of different tastants, all four species preferred sucrose as well as a mixture of sucrose and sodium chloride over MSG, and--at least at one concentration--they preferred MSG over sodium chloride. The results support the assertion that the taste responsiveness of the four primate species to MSG and sodium chloride might reflect an evolutionary adaptation to their respective dietary habits.     

Anti-predator behaviour depends on male weapon size

Tonic immobility and escape are adaptive anti-predator tactics used by many animals. Escape requires movement, whereas tonic immobility does not. If anti-predator tactics relate to weapon size, males with larger weapons may adopt tonic immobility, whereas males with smaller weapons may adopt escape. However, no study has investigated the relationship between weapon size and anti-predator tactics. In this study, we investigated the relationship between male weapon size and tonic immobility in the beetle Gnathocerus cornutus. The results showed that tonic immobility was more frequent in males with larger weapons. Although most studies of tonic immobility in beetles have focused on the duration, rather than the frequency, tonic immobility duration was not affected by weapon size in G. cornutus. Therefore, this study is the first, to our knowledge, to suggest that the male weapon trait affects anti-predator tactics.     

Comparison of rectal and tympanic core body temperature measurement in adult Guyanese squirrel monkeys (Saimiri sciureus sciureus)

Background Measuring core body temperature in a manner that is safe for animals and veterinary personnel is an important part of a physical examination. For nonhuman primates, this can involve increased restraint, additional stress, as well as the use of anesthetics and their deleterious effects on body temperature measurements. The purpose of this study was to compare two non‐invasive methods of infrared tympanic thermometry to standard rectal thermometry in adult squirrel monkeys. Methods Tympanic temperatures were collected from 37 squirrel monkeys and compared to rectal temperatures using a human and veterinary infrared tympanic thermometer. Results Compared with rectal temperature measurements, the human tympanic thermometer readings were not significantly different, while the veterinary tympanic thermometer measurements were significantly higher (P < 0.05). There were no differences between sexes. Conclusions The tympanic thermometer designed for use in humans can be used in adult squirrel monkeys as an alternative to rectal thermometry for assessing core body temperature.     

Serum and urine biochemical diversity among adult wild-caught Aotus nancymae and Saimiri peruviensis

Serum and urine analytes were compared between adult wild-caught owl monkeys (Aotus nancymae) and adult wild-caught squirrel monkeys (Saimiri peruviensis) to determine if normative clinical pathology data were similar. An objective of the study was to confirm that species of neotropical primates are distinct with regard to physiologic parameters, and should not be considered interchangeable in biomedical research. Significant differences (P < 0.05) were noted in many serum and urine analytes between the two groups. The results suggest that reference data for wild-caught owl monkeys are not applicable to squirrel monkeys, and the differences are sufficiently large to be of clinical significance. These findings illuminate the diversity among species of neotropical primates.     

Tonic immobility in terrestrial isopods: intraspecific and interspecific variability

Many arthropods, including terrestrial isopods, are capable of entering a state of tonic immobility upon a mechanical disturbance. Here we compare the responses to mechanical stimulation in three terrestrial isopods Balloniscus glaber, Balloniscus sellowii and Porcellio dilatatus. We applied three stimuli in a random order and recorded whether each individual was responsive (i.e. showed tonic immobility) or not and the duration of the response. In another trial we related the time needed to elicit tonic immobility and the duration of response of each individual. Balloniscus sellowii was the least responsive species and Porcellio dilatatus was the most, with 23% and 89% of the tested individuals, respectively, being responsive. Smaller Balloniscus sellowii were more responsive than larger individuals. Porcellio dilatatus responded more promptly than the Balloniscus spp. but it showed the shortest response. Neither sex, size nor the type of stimulus explained the variability found in the duration of tonic immobility. These results reveal a large variability in tonic immobility behavior, even between closely related species, which seems to reflect a species-specific response to predators with different foraging modes.     

Tests of planning and the Bischof-Köhler hypothesis in rhesus monkeys (Macaca mulatta)

The Bischof-Köhler hypothesis posits that nonhuman animals cannot plan for future motivational states that differ from a current state. [Naqshbandi, M., Roberts, W.A., 2006. Anticipation of future events in squirrel monkeys Samiri scireus and rats Rattus norvegicus: tests of the Bischof-Köhler hypothesis. J. Comp. Psychol. 120, 345–357] found that two squirrel monkeys that were not thirsty at the time of choice reversed their preference for a larger amount of food when choice of a smaller amount alleviated future thirst. This apparent anticipation of future thirst contradicts the Bischof-Köhler hypothesis. We used the methods described by Naqshbandi and Roberts with rhesus monkey subjects and found that the monkeys did not alter their behavior in anticipation of future thirst. To assess which factors enhance and inhibit the ability to express planning, we then systematically modified the experimental design in four subsequent experiments and found that monkeys that were not thirsty acted to alleviate future thirst only when the delay between their behavior and the contingent outcome was brief. Taken together these results suggest that the inability of rhesus monkeys to display planning resulted from their inability to learn behavior-outcome associations across long-delay intervals as would be expected from traditional accounts of operant learning, rather than from failure to anticipate future motivational states as posited by the Bischof-Köhler hypothesis.     

Genetic and phenotypic correlation between fluctuating asymmetry and two measurements of fear and stress in chickens

The purpose of the present study was to estimate the genetic and phenotypic correlation between fluctuating asymmetry and two measurements of fear and stress in chickens which had not deliberately stressed in any way, using the restricted maximum likelihood procedure. A total of 1073 36-week-old birds from two generations with complete pedigree of the Quail Castellana breed was used. Fluctuating asymmetry of several traits (leg, wing, and feather lengths, and ear-lobe and wattle areas), tonic immobility duration (indicator of fear), and heterophil to lymphocyte ratio (indicator of stress) were measured. The estimated genetic relationship between relative fluctuating asymmetry for the different traits and tonic immobility tended to be positive, that between the combined relative asymmetry of all traits and tonic immobility being near to +1; no significant phenotypic relationship was found between relative fluctuating asymmetry and tonic immobility. The genetic relationship between relative fluctuating asymmetry and heterophil to lymphocyte ratio was not consistent across the traits, ranging from +1 to −1, although the genetic correlation between the combined relative asymmetry and the heterophil to lymphocyte ratio was near to +1 too; no significant phenotypic relationship was found between relative fluctuating asymmetry and heterophil to lymphocyte ratio either. Relative fluctuating asymmetry and body weight were genetically negatively correlated for leg length and ear-lobe area but positively for feather length; the genetic correlation between the combined relative asymmetry and the body weight being near to −1; phenotypic relationships were not significantly different from zero. A significant negative genetic correlation between tonic immobility and heterophil to lymphocyte ratio was found, although the phenotypic association between these two measurements was zero. Phenotypic correlations always near to zero suggest that fluctuating asymmetry was not associated with duration of tonic immobility and heterophil to lymphocyte ratio in birds that have not been deliberately stressed.     

Tonically immobilized selfish prey can survive by sacrificing others

Death-feigning, also called tonic immobility, is found in a number of animal species across vertebrate and invertebrate taxa. To date, five hypotheses have been proposed for the adaptive significance of tonic immobility. These are that tonic immobility is effective for prey because (i) avoiding dead prey is safer for predators, (ii) immobility plays a role in physical defence, (iii) immobility plays a role in concealment and/or background matching, (iv) predators lose interest in unmoving prey, and (v) the characteristic immobilization posture signals a bad taste to predators. The fourth and fifth hypotheses have been considered suitable explanations for tonic immobility of the red flour beetle against its predator, the jumping spider. In the present study, we used chemical analyses of secretions by the red flour beetles under attack by the jumping spider to reject the fifth hypothesis for this system. More importantly, we tested a selfish-prey hypothesis for the adaptive significance of death-feigning as an anti-predator strategy, in which individuals adopting tonic immobility survive by sacrificing neighbours. Findings showed that survival rates of feigners were higher when in the presence of non-feigners or prey of a different species, compared to when alone, thus confirming our selfish-prey hypothesis. In summary, our results suggest that immobility following a spider attack is selfish; death-feigning prey increase their probability of survival at the expense of more mobile neighbours.     

Comparative normal levels of serum triiodothyronine and thyroxine in nonhuman primates.

Normative values were obtained for triiodothyronine and thyroxine from four species of Old World primate (chimpanzees, rhesus monkeys, African green monkeys and talopoin monkeys) and a single species of New World primate (squirrel monkeys) represented by two subspecies, Colombian and Bolivian. The Bolivian squirrel monkeys exhibited the lowest values for both triiodothyronine and thyroxine. Male talapoins had the highest levels of thyroxine. Significant differences were found in levels of triiodothyronine and thyroxine between males and females of the same species and between the two subspecies of squirrel monkeys. Triiodothyronine:thryroxine ratios were consistently lower in the males of all species examined.