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Distribution and ontogeny of B cells in the garden lizard, Calotes versicolor.

Surface immunoglobulin bearing (sIg+) cells were identified in the lizard Calotes versicolor by immunofluorescence using a polyvalent antiserum to lizard immunoglobulins and class-specific antibodies to lizard IgM and IgY. 53.3 +/- 1.6% of spleen cells, 23.6 +/- 0.8% of peripheral blood mononuclear cells, 21.5 +/- 1.8% of bone marrow mononuclear cells and less than 1% of thymus cells were found to bear immunoglobulin (Ig) on their surface. A similar proportion of cells in each tissue was stained with rabbit anti-lizard mu (specific for IgM) whereas only a small proportion of cells were stained with rabbit anti-lizard (specific for IgY). Adult thymectomy significantly increased the proportion of sIgM+ cells in spleen and blood whereas high dose cyclophosphamide (300mg/kg body weight) decreased the proportion of sIgM+ cells thus suggesting that sIg+ cells in the lizard are of B cell lineage as in higher vertebrates. Ontogenetic studies indicate that embryonic liver is an organ enriched for sIgM+ cells at certain stages of development and thus suggest liver to be a site for differentiation of sIg+ cells in lizard embryos.

Animals↗

The role of aldosterone in water and electrolyte transport across the colonic epithelium of the lizard, Gallotia galloti.

1. The effects of D-aldosterone on the electrical properties and ionic transport have been analysed (in vitro) in the colonic epithelium of the lizard, Gallotia galloti. 2. The injection of 30 g of D-aldosterone induced a significant rise of plasma aldosterone concentration, sustained for 4 hr after administration. 3. Intraperitoneal injections of D-aldosterone caused a slight reduction of transmural potential difference (PD) and short-circuit current (Isc). 4. Net absorption of Na+ across the colon from aldosterone-treated lizards did not increase when compared to colon from normal lizards. Cl- absorption was increased in treated lizards. 5. Addition of mucosal barium to treated tissues brought about a sustained increase of PD and Isc. 6. The absorption of fluid in normal lizards was reversed to fluid secretion in treated lizards. 7. The effects of D-aldosterone on lizard colon are compared with those reported for the colon of mammals and birds.

Aldosterone↗

Oxidative DNA damage and antioxidant defenses in the European common lizard (Lacerta vivipara) in supercooled and frozen states.

The European common lizard (Lacerta vivipara) tolerates long periods at sub-zero temperatures, either in the supercooled or the frozen state. Both physiological conditions limit oxygen availability to tissues, compelling lizards to cope with potential oxidative stress during the transition from ischemic/anoxic conditions to reperfusion with aerated blood during recovery. To determine whether antioxidant defenses are implicated in the survival of lizards when facing sub-zero temperatures, we monitored the activities of antioxidant enzymes and oxidative stress either during supercooling or during freezing exposures (20 h at -2.5 degrees C) and 24 h after thawing in two organs of lizards--muscle and liver. Supercooling induced a significant increase in the total SOD and GPx activity in muscle (by 67 and 157%, respectively), but freezing had almost no effect on enzyme activity, either in muscle or in liver. By contrast, thawed lizards exhibited higher GPx activity in both organs (a 133% increase in muscle and 59% increase in liver) and a significant decrease in liver catalase activity (a 47% difference between control and thawed lizards). These data show that supercooling (but not freezing) triggers activation of the antioxidant system and this may be in anticipation of the overgeneration of oxyradicals when the temperature increases (while thawing or at the end of supercooling). Oxidative stress was assessed from the content of 8-oxodGuo and the different DNA adducts resulting from lipid peroxidation, but it was unaltered whatever the physiological state of the lizards, thus demonstrating the efficiency of the antioxidant system that has been developed by this species. Overall, antioxidant defenses appear to be part of the adaptive machinery for reptilian tolerance to sub-zero temperatures.

Adaptation, Physiological↗

Refuge use: a conflict between avoiding predation and losing mass in lizards.

Prey often respond to predation risk by increasing refuge use, but this strategy may entail a loss of body condition. Factors responsible for this loss of body condition remain unclear. Also how prey deal with refuge use to cope with predation risk without incurring costs of body condition, and how initial body condition affects refuge use remain barely known. We analyzed in the field whether adult Iberolacerta cyreni lizards modify their escape strategies and refuge use in areas with different levels of habitat deterioration and ecotourism pressure, which represent different levels of predation risk, and the consequences of changes in antipredator behavior to body condition. Lizards inhabiting deteriorated areas, where risk is higher, remained closer to refuges, but decreased time spent hidden in refuges after attacks, probably to maintain similar body condition than lizards inhabiting natural areas. We performed two laboratory experiments to isolate potential costs of refuge use that might affect the body condition of male lizards: a) a decrease of the efficiency of digestion due to low temperatures inside refuges and/or b) a reduction in food intake. Results suggest that refuge use is costly in terms of body condition due to reduced food intake, but the loss of efficiency of digestion seems unimportant. Lizards modified refuge use in relation to their body condition, with lizards with worse condition decreasing time hidden after predatory attacks. We concluded that lizards compensated for increased predation risk with flexible antipredatory strategies, coping with risk without incurring costs for body condition.

Adaptation, Physiological↗

Abundance of ticks (Acari: Ixodidae) infesting the western fence lizard, Sceloporus occidentalis, in relation to environmental factors.

We examined the impact of environmental characteristics, such as habitat type, topographic exposure and presence of leaf litter, on the abundance of Ixodes pacificus ticks infesting the western fence lizard (Sceloporus occidentalis) at the University of California Hopland Research and Extension Center (HREC), Mendocino County, California. A total of 383 adult lizards were slip-noosed and examined for tick infestation in April and May 1998. At least 94% of the lizards were infested by ticks and at least 20% of the females and 33% of the males carried > 15 ticks. This intensive utilization of western fence lizards (which do not serve as natural reservoirs for Lyme disease spirochetes) by subadult ticks, is probably the primary reason for the low prevalence of infection with Borrelia burgdorferi in I. pacificus nymphs and adults previously recorded at the HREC. Tick loads were higher on male than female lizards. Also, male lizards were generally more heavily infested in late April than in late May. The prevalence of tick infestation exceeded 88% in all habitat types but males collected in woodland and grass/woodland edges had higher tick loads than those collected in open grassland. Male lizards captured in open, exposed grassland tended to carry heavier tick loads in northern/eastern, as compared to southern/western, exposures, and when leaf litter was present.

Animals↗

Low cost of locomotion in lizards that are active at low temperatures.

The nocturnality hypothesis of K. Autumn and coworkers states that nocturnal geckos have evolved a low energetic cost of locomotion (C(min)). A low C(min) increases maximum aerobic speed and partially offsets the decrease in maximum oxygen consumption caused by activity at low nocturnal temperatures. We tested whether a low C(min) is unique to nocturnal geckos or represents a more general pattern of convergent evolution among lizards that enables nocturnality and/or cold-temperature activity. We measured C(min) in four carefully selected lizard species from New Zealand (two nocturnal and two diurnal; n=5-9 individuals per species), including a nocturnal and diurnal gecko (a low C(min) is a gecko trait and is not related to nocturnality), a nocturnal skink (a low C(min) is related to being nocturnal), and a diurnal skink active at low temperatures (a low C(min) is related to being active at low body temperatures). The C(min) values of the four species measured in this study (range=0.21-2.00 mL O(2) g(-1) km(-1)) are lower than those of diurnal lizards from elsewhere, and the values are within or below the 95% confidence limits previously published for nocturnal geckos. A low C(min) increases the range of locomotor speeds possible at low temperatures and provides an advantage for lizards active at these temperatures. We accepted the hypothesis that nocturnal lizards in general have a low C(min) and provide evidence for a low C(min) in lizards from cool-temperate environments. The low C(min) in lizards living at high latitudes may enable extension of their latitudinal range into otherwise thermally suboptimal habitats.

Animals↗

Daily and seasonal rhythms in selected body temperatures in the Australian lizard Tiliqua rugosa (Scincidae): field and laboratory observations.

This study examined daily and seasonal activity and thermoregulatory behaviour of the sleepy lizard, Tiliqua rugosa, a large, diurnally active temperate-dwelling Australian lizard, in the field and laboratory. Activity temperatures in the field were compared with those selected by lizards in laboratory thermal gradients in order to assess the extent to which endogenous versus exogenous factors contribute to seasonal variations in thermoregulatory behaviour. In the field, lizards are most active in late winter-spring (August-November), during which their activity varies from mostly unimodal on days of mild temperature to bimodal on hot days. In late spring-summer (November-January), activity is largely restricted to early morning, and at all other seasons sleepy lizards are rarely active. The winter-spring activity of sleepy lizards is constrained by low environmental temperatures, as lizards at these seasons have low body temperatures in the field but higher temperatures in laboratory thermal gradients. The lower temperatures selected in the laboratory in the summer-autumn months suggest the avoidance of high ambient temperatures and general inactivity in the field at these times. Thermal selection in the laboratory at the eight times of year tested showed that the phase of the minimum and maximum temperature selected and the amplitude of the rhythm of temperature selected varied continuously with the time of year. These daily and seasonal shifts in thermoregulatory behaviour may be regulated by endogenous physiological mechanisms coupled with seasonal ecological constraints such as food availability.

Animals↗

Lyme disease in California: interrelationship of Ixodes pacificus (Acari: Ixodidae), the western fence lizard (Sceloporus occidentalis), and Borrelia burgdorferi.

The relationship of immature western black-legged ticks, Ixodes pacificus Cooley and Kohls, to the western fence lizard, Sceloporus occidentalis Baird and Girard, and to the Lyme disease spirochete, Borrelia burgdorferi, was investigated in chaparral and woodland-grass habitats in northern California from 1984 to 1986. Immature ticks were found on lizards in spring and summer, but the prevalence and abundance of ticks on this host were considerably greater in spring. The peak of larval abundance preceded that of nymphs by several weeks, but there was considerable seasonal overlap between these parasitic stages. Larvae and nymphs attached primarily to the lateral nuchal pockets of lizards in chaparral (99.5%) and woodland-grass (91.8%). The numbers of larvae infesting lizards in spring fit the negative binomial distribution in woodland-grass but not in chaparral; insufficient data precluded similar analyses for nymphs. Tick loads did not differ significantly with respect to age or gender of the lizard. Spirochetal infection rates (range, 0-3.7%) in I. pacificus immatures were comparable in both habitats and were similar to those reported previously for adults of this tick. Overall, 1 (0.9%) of 117 larvae and 10 (1.8%) of 552 nymphs were infected with spirochetes resembling B. burgdorferi. Spirochetes were not observed in blood smears prepared from 261 wild-caught lizards, including five lizards fed upon by infected ticks at the time of collection. These and other findings suggest that S. occidentalis, although an important host of I. pacificus immatures, may be less important as a source for infecting ticks with B. burgdorferi.

Animals↗

Infestation of the southern alligator lizard (Squamata: Anguidae) by Ixodes pacificus (Acari: Ixodidae) and its susceptibility to Borrelia burgdorferi.

To investigate the reservoir potential of the southern alligator lizard, Elgaria multicarinata (Blainville), for the Lyme disease spirochete, Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt & Brenner, 14 lizards were collected from 1 county on each side of the northern Central Valley of California. Seven animals were collected from a Placer County site (Drivers Flat) and a Yolo County site (Cache Creek) where B. burgdorferi had been isolated previously from Ixodes pacificus Cooley & Kohls. Overall, the mean abundance of I. pacificus on all 14 lizards was 34.1 (range, 3-63) for larvae and 11.0 (range, 1-28) for nymphs. In captivity, field-attached I. pacificus larvae and nymphs required, on average, 12.6 (range, 1-37) and 14.4 (range, 5-44) d to feed to repletion, respectively. The prevalence of B. burgdorferi infection in host-seeking I. pacificus nymphs was 1.4% in Cache Creek Canyon and 9.9% in Drivers Flat. Attempts to isolate spirochetes from lizard blood or ticks that had fed on lizards and subsequently molted were unsuccessful as were efforts to cultivate spirochetes in lizard sera. These data suggest that the southern alligator lizard is not a competent reservoir for B. burgdorferi, although it is an important host for I. pacificus subadults.

Animals↗

Perpetuation of the Lyme disease spirochete Borrelia lusitaniae by lizards.

To determine whether the Lyme disease spirochete Borrelia lusitaniae is associated with lizards, we compared the prevalence and genospecies of spirochetes present in rodent- and lizard-associated ticks at a site where this spirochete frequently infects questing ticks. Whereas questing nymphal Ixodes ricinus ticks were infected mainly by Borrelia afzelii, one-half of the infected adult ticks harbored B. lusitaniae at our study site. Lyme disease spirochetes were more prevalent in sand lizards (Lacerta agilis) and common wall lizards (Podarcis muralis) than in small rodents. Although subadult ticks feeding on rodents acquired mainly B. afzelii, subadult ticks feeding on lizards became infected by B. lusitaniae. Genetic analysis confirmed that the spirochetes isolated from ticks feeding on lizards are members of the B. lusitaniae genospecies and resemble type strain PotiB2. At our central European study site, lizards, which were previously considered zooprophylactic for the agent of Lyme disease, appear to perpetuate B. lusitaniae.

Animals↗

Plasma iron, copper, and zinc in lizard Dipsosaurus dorsalis: effects of bacteria injection.

The effects of inoculation of desert iguanas (Dipsosaurus dorsalis) with heat-killed Aeromonas hydrophila on the plasma concentrations of iron, copper, and zinc, and the total iron-binding capacity have been determined. Plasma iron concentration and total iron-binding capacity fell significantly in inoculated lizards maintained at temperatures corresponding to those selected during fever. Plasma copper concentration did not change in response to inoculation (as determined at 24 h postinjection). Plasma zinc concentration fell in inoculated lizards regardless of whether the lizards were maintained at temperatures corresponding to those selected by afebrile or febrile lizards. There were no effects of varying the zinc concentration (corresponding to those observed in noninfected lizards, infected lizards, or at subnormal levels) on the in vitro growth rate of A. hydrophila. We hypothesize that the reduction in plasma zinc observed in infected mammals, and now in infected lizards, may have an effect (perhaps by some indirect pathway) on the in vivo growth rate of A. hydrophila.

Aeromonas↗

Pyrogens fail to produce fever in a cordylid lizard.

We investigated the effects on body temperature of the lizard Cordylus cataphractus of intracardiac injections of leucocyte pyrogen (LP) synthesized from rabbit blood and of killed Aeromonas hydrophila, a gram-negative bacterium reputed to be pathogenic in lizards. Lizards were placed in a photothermal gradient that allowed them to select a preferred body temperature following the injections. Neither injection of 0.5 ml rabbit LP nor of 4 X 10(9) organisms of A. hydrophila in 0.2 ml sterile saline caused body temperature of lizards to differ from that of control lizards injected with sterile saline. Following injection of these solutions in the lizards placed in a thermal gradient where ambient temperature ranged from 20-88 degrees C, body temperature was maintained between 32 and 34 degrees C. Pyrogens failed to elevate body temperature even when body temperature was elevated artificially to 36 degrees C before injection. We conclude that C. cataphractus does not respond with fever to either rabbit LP or A. hydrophila. Fever may not be ubiquitous even among lizards.

Aeromonas↗

Convergence of thalamic and cholinergic projections in the 'dentate area' of lizards.

The small-celled part of the medial cortex (Cxms) in lizards is comparable to the hippocampal area dentata in mammals. As in mammals, most of the afferents to this cortical area are arranged in sharply delimited laminae. In reptiles this lamination pattern is species-specific. In the lizard Tupinambis nigropunctatus projections from the multisensory dorsolateral thalamic nucleus (Dla) terminate in the middle one-third of the outer plexiform layer throughout the whole rostrocaudal extent of Cxms. In Podarcis hispanica the thalamic projections terminate not only in the middle one-third of Cxms but also in the inner plexiform layer. To find out whether the species-related variation of thalamic projections to Cxms is a solitary phenomenon or is related to variations of other afferents of Cxms, we studied the relationships between the thalamic and cholinergic projections from the basal telencephalon in the medial cortex of three lizard families: the Lacertidae, the Teiidae and the Gekkonidae. In the gekkonid lizards Gekko gecko and Eublepharius macularius, Dla projections were studied with the anterograde tracer Phaseolus vulgaris-leucoagglutinin. Projections were found in only the rostral one-third of Cxms where the fibers terminate in the superficial half of the outer plexiform layer and in the deep half of the inner plexiform layer. From acetylcholinesterase staining in the Cxms of representatives of these three lizard families, it appeared that the main cholinergic afferents terminate in the same subregions and the same laminae as the Dla projections. Therefore, there seems to be a close association between thalamic and cholinergic afferents in the Cxms of lizards, irrespective of their precise location in the cortex of the various species. This suggests a functional relationship between these two afferents of the dentate area in lizards.

Acetylcholinesterase↗

Prey snapping and visual distance estimation in Texas horned lizards, Phrynosoma cornutum.

Captive Texas horned lizards were high-speed videotaped while feeding on ants in order to study the role of vision in facilitating tongue-protrusion capture of prey. Analysis of tongue movements revealed that prey snapping in these lizards is not a typical fixed-action pattern. By contrast, it is variable in performance and duration. Lizards adjusted head and tongue direction during the strike, within a few milliseconds, in response to movements of the prey. The duration of a typical tongue strike was 100-150 ms. The strike duration was prolonged after ophthalmic lenses were placed in front of one or both eyes. These lenses were used to investigate whether horned lizards use accommodation to judge prey distance. Focal changes of negatively powered ophthalmic lenses (employed monocularly) induced a clear underestimation of prey distance by the lizards, confirming the hypothesized expectation that accommodation is used for depth perception. The effect of the lenses was different in the two animals tested with monocular restriction. This, together with the lack of difference in responses by the lizards when untreated and when both eyes were lens covered (binocular treatment of equal power, -9 D), illustrates that horned lizards also use other visual parameters for depth perception.

Accommodation, Ocular↗

Prey capture kinematics of ant-eating lizards.

While morphological and behavioral feeding specializations are obvious in many vertebrate groups, among lizards there appear to be few dietary specialists. By comparing the prey capture kinematics and overall feeding behavior in two highly specialized ant-eating lizards (Moloch horridus and Phrynosoma platyrhinos) with those of two closely related dietary generalists (Pogona vitticeps and Uma notata), we investigate whether dietary specialization has been accompanied by changes in the function and use of the feeding system. We quantified kinematic variables from high-speed video recordings (200-250 frames s(-1)) of each species feeding on ants. Prey capture was strikingly different in M. horridus to that of other species, being characterized by a suite of unusual behaviors including the lack of a body lunge, faster tongue protrusion, reduced prey processing and, most notably, the ability to modulate the slow open phase of the gape cycle. In concert, these traits make a single feeding event in M. horridus faster than that in any other iguanian lizard studied to date. Prey capture behavior in P. platyrhinos is kinematically more similar to U. notata and P. vitticeps than to M. horridus, but the ant specialists are similar in that both lack distinct prey processing behaviors, resulting in faster overall capture and feeding events. While ant feeding in P. vitticeps is faster than feeding on other prey, the duration of a single feeding event is still four times longer than in either ant specialist, because of extensive prey processing. Additionally, a phylogenetic comparison of ant specialist lizards with dietary generalists revealed that ant-eating lizards require significantly less time to capture and process prey. Thus there are not only significant behavioral modifications in these ant-eating lizards, but also multiple strategies among specialists, suggesting differing selective pressures or phylogenetic constraints in the evolution of ant eating in lizards.

Animals↗

Prevalence and abundance of Ixodes pacificus immatures (Acari: Ixodidae) infesting western fence lizards (Sceloporus occidentalis) in northern California: temporal trends and environmental correlates.

The prevalence and abundance of immature Ixodes pacificus ticks on western fence lizards (Sceloporus occidentalis) were examined in relation to time of year, host attributes (i.e., age, gender, and presence or absence of blood parasites), and 5 environmental characteristics, including topographic exposure and ground cover substrate, over a 2-year period in northern California. Lizards were infested with subadult ticks from early March until late July or early August, with peak median numbers of larvae and nymphs recorded in late April and early May of both years. Peak larval and nymphal abundances differed between years. The overall ratio of larvae to nymphs on adult male lizards was low, ranging from 0.80 in 1999 to 2.41 in 2000. Such intensive feeding of nymphs versus larvae on these lizards, which are reservoir-incompetent for Borrelia burgdorferi spirochetes, may explain previous observations of decreasing spirochetal infection prevalence from the nymphal to adult stage in northwestern California. Adult male lizards were more likely to be infested with nymphs and harbored greater abundances of larvae and nymphs than adult females. Lizards uninfected with blood parasites had more nymphs than infected lizards. The measured environmental characteristics could explain only a small percentage of the total variation observed in larval prevalence (22%) and in larval and nymphal abundance (12 and 3%, respectively).

Animals↗

Retinal projections throughout optic nerve regeneration in the ornate dragon lizard, Ctenophorus ornatus.

In goldfish and frog, optic nerve regeneration is successful, with restoration of retinotopic projections in visual brain centres and the return of functional vision within 1-2 months. By contrast, at 1 year after unilateral optic nerve crush in the ornate dragon lizard (Ctenophorus ornatus), the regenerated retinotectal projections lack topographic order, presumably explaining why the lizards are blind via the experimental eye (Beazley et al. [1997] J. Comp. Neurol. 377:105-120). To determine whether other abnormalities are associated with the inability to restore topographic projections in the lizard, we charted anatomically the time course, accuracy, and stability of optic nerve regeneration by examining visual projections with the lipophillic dye 1,1'-dioctadecyl-3,3,3', 3'-tetramethylindocarbocyanine perchlorate (DiI) applied to the optic disk at intervals up to 1 year after optic nerve crush; in addition, DiI tracing of small groups of axons was used to examine the topicity of axons projecting to the tectum. Axons re-innervated visual centres from between 1 and 2 months, a time frame comparable with that in goldfish and frog. However, the projections in lizard were found to differ from those in goldfish and frog in three major ways. First, there was considerable variability within the projection patterns both between individual lizards at any one stage and with time. Second, the projections were inaccurate. As in normal lizards, the major projection was to the contralateral optic tectum, although it lacked detectable retinotopic axon order throughout. Furthermore, misrouting occurred such that regenerating axons formed a persistent projection to the ipsilateral side of the brain that was considerably stronger and more widespread than normal. Minor visual centres also became re-innervated but, in addition, regenerating axons formed persistent projections into the opposite optic nerve and to non-retino-recipient regions such as the nucleus rotundus, hypothalamus, and olfactory nerve, as well as the posterior and tectal commissures. Third, the projections appeared unstable. Projections to both tecta were strongest between 3 and 5 months, but they diminished thereafter. The results suggest that, compared with goldfish and frog, in lizards both pathway and target cues are degraded and/or cannot be read adequately; as a consequence, regenerating axons are unable to navigate exclusively to visual centres and cannot re-form stable connections.

Animals↗

Responses to chemical cues from animal and plant foods by actively foraging insectivorous and omnivorous scincine lizards.

If tongue-flicking is important to lizards to sample chemical cues permitting identification of foods, tongue-flicking and subsequent feeding responses should be adjusted to match diet. This hypothesis can be examined for plant foods because most lizards are insectivores, but herbivory/omnivory has evolved independently in many lizard taxa. Here we present experimental data on chemosensory responses to chemical cues from animal prey and palatable plants by three species of the scincine lizards. When tested with chemical stimuli presented on cotton swabs, the insectivorous Eumeces fasciatus responded strongly to prey chemicals but not to chemicals from plants palatable to omnivorous lizards or to pungent or odorless control stimuli. Two omnivorous species, E. schneideri and Scincus mitranus, responded more strongly to chemical cues from both prey and food plants than to the control chemicals. All available data for actively foraging lizards, including these skinks, show that they are capable of prey chemical discrimination, and insectivores do not exhibit elevated tongue-flicking or biting responses to chemical cues from palatable plants. In all of the several species of herbivores/omnivores tested, the lizards show elevated responses to both animal and plant chemicals. We suggest two independent origins of both omnivory and plant chemical discrimination that may account for the evolution of diet and food chemical discriminations in the eight species of skinks studied, five of which are omnivores. All data are consistent with the hypothesis that acquisition of omnivory is accompanied by acquisition of plant chemical discrimination, but data on a broad diversity of taxa are needed for a definitive comparative test of the evolutionary hypothesis. J. Exp. Zool. 287:327-339, 2000.

Animals↗