Sexual differences in caudal morphology and its relation to tail autotomy in lacertid lizards

We hypothesized that the presence of the forked hemipenes, and associated musculature, at the base of the tail in male lizards should constrain the capacity to autotomize the tail. Thus, this hypothesis predicts that the non-autotomous base of the tail should be longer in male than in female lizards. We tested this hypothesis in four species oflacertid lizards. Males have on average one to two non-autotomous vertebrae more than females, and the sexual difference in length of the non-autotomous tail base remains constant over the entire body size range. In addition, the first functional autotomy plane in males is usually located on, or is distal to, the vertebrae from which two hemipenial muscles take origin. These observations support the view that functional demands of the male intromittent organs impose constraints on the abilities of tail autotomy. In a natural population of Lacerta vivipara , the proportion of tail breaks that occurred at very short distances from the base was highest in females, indicating that the small sexual difference in length of the non-autotomous tail part is of functional significance. Total length of the tail was largest in males. This can be interpreted as a compensation for the decline in autotomy capacities at the tail base, such that the length of the autotomous part remains similar in both sexes.     

The energetic costs of tail autotomy to reproduction in the lizard Coleonyx brevis (Sauria: Gekkonidae)

Summary Energy reserve utilization and energy budgets were compared in tailed and tailless adult female Coleonyx brevis. Carcass, fat body and caudal energy reserves were used for vitellogenesis; mass and energy content (cal/mg and/or cal/reserve) of each were significantly lower at oviposition than at the initiation of vitellogenesis. Total energy reserves accounted for 53% of the reproductive energy investment in tailed females compared to 29% in tailless females. Tailed females had over twice as many reserve calories for egg production than tailless females. Caudal energy reserves represented 60% of the total reserves of tailed females and were one-third greater than the total energy reserves of tailless females. To produce a clutch of eggs both tailed and tailless females supplemented energy reserves with net metabolizable energy that was available after metabolic costs were paid. Tailless females had a significantly greater rate of food ingestion and more net metabolizable energy available for reproduction than tailed females, yet allocated significantly fewer calories/day to reproduction than tailed females, primarily because of the loss of caudal reserves. Reproductive efforts of tailed and tailless females were equivalent. However, the loss of caudal reserves resulted in the production of eggs that were significantly lower in mass and energy content (cal/mg and cal/egg) than when caudal reserves were used. Results empirically support the hypothesis that reproduction has energetic priority over tail regeneration in short-lived, iteroparous species with a low probability of future reproductive success.     

Caudal autotomy and regeneration in lizards

Caudal autotomy, or the voluntary self-amputation of the tail, is an anti-predation strategy in lizards that depends on a complex array of environmental, individual, and species-specific characteristics. These factors affect both when and how often caudal autotomy is employed, as well as its overall rate of success. The potential costs of autotomy must be weighed against the benefits of this strategy. Many species have evolved specialized behavioral and physiological adaptations to minimize or compensate for any negative consequences. One of the most important steps following a successful autotomous escape involves regeneration of the lost limb. In some species, regeneration occurs rapidly; such swift regeneration illustrates the importance of an intact, functional tail in everyday experience. In lizards and other vertebrates, regeneration is a highly ordered process utilizing initial developmental programs as well as regeneration-specific mechanisms to produce the correct types and pattern of cells required to sufficiently restore the structure and function of the sacrificed tail. In this review, we discuss the behavioral and physiological features of self-amputation, with particular reference to the costs and benefits of autotomy and the basic mechanisms of regeneration. In the process, we identify how these behaviors could be used to explore the neural regulation of complex behavioral responses within a functional context.     

Functional morphology and evolution of tail autotomy in salamanders

Basal tail constriction occurs in about two-thirds of the species of plethodontid salamanders. The constriction, which marks the site of tail autotomy, is a result of a reduction in length and diameter of the first caudal segment. Gross and microscopic anatomical studies reveal that many structural specializations are associated with basal constriction, and these are considered in detail. Areas of weakness in the skin at the posterior end of the first caudal segment, at the attachment of the musculature to the intermyotomal septum at the anterior end of the same segment, and between the last caudosacral and first caudal vertebrae precisely define the route of tail breakage. During autotomy the entire tail is shed, and a cylinder of skin one segment long closes over the wound at the end of the body. It is suggested that specializations described in this paper have evolved independently in three different groups of salamanders. Experiments and field observations reveal that, contrary to expectations, frequency of tail breakage is less in species with apparent provisions for tail autotomy than in less specialized species. The tail is a very important, highly functional organ in salamanders and it is suggested that selection has been for behavioral and structural adaptations for control of tail loss, rather than for tail loss per se.     

The m. caudifemoralis longus and its relationship to caudal autotomy and locomotion in lizards (Reptilia: Sauna)

Although the phenomenon of tail autotomy has traditionally been viewed in a purely adaptive light, functional constraints imposed by the locomotor system appear to have influenced the presence and extent of autotomy in lizards. Them. caudifemoralis longus is an unsegmented hind limb retractor that originates from the caudal vertebrae. It does not participate in autotomy and thus limits the proximal position of autotomic septa. Variation in the extent of the m. caudifemoralis is correlated with locomotor type. The muscle is large and originates from a long series of caudal vertebrae in fast moving lizards with powerful limb retraction, as exemplified by taxa capable of bipedal running. In slower lizards with sprawling postures, such as geckos, the m. caudifemoralis is small and restricted to the first few postsacral vertebrae. Autotomy is typically restricted or absent in the former lizards, while in the latter only the most proximal vertebrae are incapable of autotomy. In the evolution of existing patterns of caudal autotomy, functional demands intrinsic to the tail may be subservient to locomotor constraints imposed on the tail base by the m. caudifemoralis longus .     

The process of total tail autotomy in the South-American rodent, Proechimys

Tail autotomy in Proechimys cuvieri was studied both morphologically and histologically. The rupture always occurs at the base of the external tail, e.g. in the immediate vicinity of its junction with the body. It thus concerns the whole caudal appendage. The distal epiphysis is separated from the fifth caudal vertebra and lost with the rest of the tail. There is no single reason responsible for the constancy of this breaking point, but several morphological factors can act together: these include strong binding of the five first caudal vertebrae to the body, disappearance of the plurisegmental muscles beyond this level, and the great extent and loose structure of the epiphyseal plates. Autotomy is a biological event occurring throughout the life of the animals, but it is of a cumulative nature. Tail loss is much more prevalent in older and heavier animals than in juveniles. Overall, about 9% of wild populations show this loss. Owing to the increasing percentage of occurrence from young to old, tail autotomy seems to enhance the survival chances of its owner, although direct proof of any predation influence are still lacking.     

Arm autotomy in brittlestars (Echinodermata: Ophiuroidea)

Although ophiuroid arm shedding has long been accepted as an example of autotomy, there has been little investigation of the phenomenon to substantiate this. This paper describes the outwardly visible aspects of autotomy and the function of the internal components of the arm during detachment. Observations are focussed on Ophiocomina nigra, some comparisons being made with eight other species.
Ophiuroid autotomy is characterized by its occurrence close to the point of stimulation, its rapidity, and by the pattern of intervertebral muscle separation at the insertions which is constant for a given species. Evidence is presented showing the important role played by the intervertebral ligament. Both this and the muscle insertions are collagenous, and it is suggested that they and the other intersegmental connective tissues facilitate autotomy by undergoing a drastic, nervously mediated loss in tensile strength which enables the animal to part from its arm with a minimum of effort. Comparable properties have been ascribed to other echinoderm connective tissues, and their role in asteroid and holothurian autotomy has been acknowledged, but such a mechanism has not previously been suggested for ophiuroid arm autotomy.     

Autocrine and paracrine Shh signaling are necessary for tooth morphogenesis, but not tooth replacement in snakes and lizards (Squamata)

Here we study the role of Shh signaling in tooth morphogenesis and successional tooth initiation in snakes and lizards (Squamata). By characterizing the expression of Shh pathway receptor Ptc1 in the developing dentitions of three species (Eublepharis macularius, Python regius, and Pogona vitticeps) and by performing gain- and loss-of-function experiments, we demonstrate that Shh signaling is active in the squamate tooth bud and is required for its normal morphogenesis. Shh apparently mediates tooth morphogenesis by separate paracrine- and autocrine-mediated functions. According to this model, paracrine Shh signaling induces cell proliferation in the cervical loop, outer enamel epithelium, and dental papilla. Autocrine signaling within the stellate reticulum instead appears to regulate cell survival. By treating squamate dental explants with Hh antagonist cyclopamine, we induced tooth phenotypes that closely resemble the morphological and differentiation defects of vestigial, first-generation teeth in the bearded dragon P. vitticeps. Our finding that these vestigial teeth are deficient in epithelial Shh signaling further corroborates that Shh is needed for the normal development of teeth in snakes and lizards. Finally, in this study, we definitively refute a role for Shh signaling in successional dental lamina formation and conclude that other pathways regulate tooth replacement in squamates.     

Multiple C-terminal tail Ca(2+)/CaMs regulate Ca(V)1.2 function but do not mediate channel dimerization

Interactions between voltage-gated calcium channels (Ca(V)s) and calmodulin (CaM) modulate Ca(V) function. In this study, we report the structure of a Ca(2+)/CaM Ca(V)1.2 C-terminal tail complex that contains two PreIQ helices bridged by two Ca(2+)/CaMs and two Ca(2+)/CaM-IQ domain complexes. Sedimentation equilibrium experiments establish that the complex has a 2:1 Ca(2+)/CaM:C-terminal tail stoichiometry and does not form higher order assemblies. Moreover, subunit-counting experiments demonstrate that in live cell membranes Ca(V)1.2s are monomers. Thus, contrary to previous proposals, the crystallographic dimer lacks physiological relevance. Isothermal titration calorimetry and biochemical experiments show that the two Ca(2+)/CaMs in the complex have different properties. Ca(2+)/CaM bound to the PreIQ C-region is labile, whereas Ca(2+)/CaM bound to the IQ domain is not. Furthermore, neither of lobes of apo-CaM interacts strongly with the PreIQ domain. Electrophysiological studies indicate that the PreIQ C-region has a role in calcium-dependent facilitation. Together, the data show that two Ca(2+)/CaMs can bind the Ca(V)1.2 tail simultaneously and indicate a functional role for Ca(2+)/CaM at the C-region site.     

Lethal and sublethal costs of autotomy and predator presence in damselfly larvae

We studied the costs of lamellae autotomy with respect to growth and survival of Lestes sponsa damselfly larvae in field experiments. We manipulated predation risk by Aeshna cyanea dragonfly larvae and lamellae status of L. sponsa larvae in field enclosures and compared differences in numbers, size and mass of survivors among treatments. In the absence of a free-ranging A. cyanea larva, about 29% of the L. sponsa larvae died. This was probably due to cannibalism. The presence of a free-ranging A. cyanea reduced larval survival by 68% compared to treatments in which it was absent or not permitted to forage on L. sponsa damselflies. Across all predator treatments, lamellae autotomy reduced survival by about 20%. The mean head width and mass of survivors was lower in the enclosures with a free-ranging A. cyanea compared to the other two predator treatments. This suggested that larvae grew less in the presence of a free-ranging predator, indicating that increased antipredator behaviours were more important in shaping growth responses than reduced population density. Mass, but not head width, of survivors was also reduced after autotomy. The fitness consequences of these effects for the adults may be pronounced. In general, these field data strongly suggest that lamellae autotomy affects population regulation of damselflies. Received: 1 February 1999 / Accepted: 22 March 1999     

Energetic costs of activity by lizards in the field

1. The available data related to the activity energetics of lizards in the field were collated with respect to three indices of activity energetics: the ecological cost of transport (ECT) expressed as a percentage of the total energy, the proportion of total energy used in all forms of activity (%AR), and the sustained metabolic scope (SusMS), defined as the ratio of the total energy expenditure to the total resting metabolism.
2. The ECT values of lizards ranged from 3 to 36% with five of 11 species having values >20%. The percentage AR ranged from 23 to 80% for lizards during active seasons, with most species having values > 50%. The SusMS ranged from 1·1 to 5·1.
3. Values of ECT are higher for lizards than for mammals, in part because the costs of maintenance metabolism are higher in mammals.
4. The percentage AR and SusMS values of mammals are higher than those of lizards.
5. It follows from the previous two points that the proportion of the total daily energy that is expended in non-locomotory activities is disproportionately higher in mammals compared with lizards.
6. The energy expended in locomotion is a significant portion of the energy budget of lizards. This is generally true for all seasons in which there is activity.     

Tail autotomy and extinction in Mediterranean lizards. A preliminary study of continental and insular populations

Tail autotomy is one of the main anti-predator mechanisms of lacertid lizards, but it has been predicted that it is only retained in its full capacity when its benefits exceed its costs (Arnold, 1988). To test this hypothesis, ease of tail shedding was examined in a number of continental and insular lacertid lizard populations, each of which showed a different shedding capacity. Tails are shed more easily in those continental and insular populations where there is a greater probability of predation. In insular populations not subjected to strong predation, the tail tends to be retained. The relationship of these findings to insular Mediterranean lizard populations and to the extinction of the Balearic lizard, Podarcis lilfordi are discussed.     

Leg autotomy in a spider has minimal costs in competitive ability and development

A number of species have the ability to autotomize limbs voluntarily, but animals that have lost limbs often face substantial costs. We examined the frequency of leg loss and its effects on competitive ability and development in the spider Holocnemus pluchei (Araneae: Pholcidae), a family of spiders known for its readiness to autotomize legs. Leg loss was common in field populations, with 7.5% of all surveyed spiders missing at least one leg, most commonly one of the anterior pair. More spiders were missing multiple legs than expected by chance, suggesting that leg loss events are not independent. Large adult spiders were missing legs more frequently than were small spiders. The competitive ability of injured males was tested in three contexts. In the field, no effect of leg loss was found on the ability of spiders to remain in webs into which they were introduced. In the laboratory, no effect of leg loss was found on the ability to fight with a single opponent over a prey, except that injured spiders were more likely to lose high-intensity fights. There was no difference between intact and injured males in their ability to compete with three females for limited prey. Leg loss significantly affected development time. The moult interval during the instar in which the injury occurred increased by approximately 15%. However, the growth rate for injured spiders was slightly but not significantly faster in the instar following leg loss, and total development time of the two instars together did not differ significantly between treatments. No spider showed any signs of regeneration. We conclude that, although there were some statistically significant differences between intact and injured males, these are unlikely to have major impacts on fitness, in contrast to findings in other species. Copyright 1999 The Association for the Study of Animal Behaviour.     

北京幽灵蛛的附肢自残

附肢自残是北京幽灵蛛（Pholcus beijingensis Zhu ＆ Song,1999）的习性之一。野外调查表明,约20％的个体至少失去1只步足;个体自残的发生率在2—7月间有显著的差异,同时第一对步足自残的比例最高（43．47％）;个体失去步足的比例随着年龄的增加而增加;左侧和右侧步足失去的比率接近（1．03：1）。野外调查发现,正在交配的个体与单独生活的个体相比,步足的完整性上并无显著差别。实验室研究表明,北京幽灵蛛附肢自残后没有再生现象。通过对自残幼体与非自残幼体的3龄与4龄龄期研究,发现各处理组间并无显著的差别。步足自残被认为是北京幽灵蛛在极端情况下的“避险策略”（Bet-hedging strategy）[动物学报54（6）：998-1004,2008]。     

Synorganisation without organ fusion in the flowers of Geranium robertianum (Geraniaceae) and its not so trivial obdiplostemony

Background and Aims

Synorganisation of floral organs, an important means in angiosperm flower evolution, is mostly realized by congenital or post-genital organ fusion. Intimate synorganisation of many floral organs without fusion, as present in Geranium robertianum, is poorly known and needs to be studied. Obdiplostemony, the seemingly reversed position of two stamen whorls, widely distributed in core eudicots, has been the subject of much attention, but there is confusion in the literature. Obdiplostemony occurs in Geranium and whether and how it is involved in this synorganisation is explored here.

Methods

Floral development and architecture were studied with light microscopy based on microtome section series and with scanning electron microscopy.

Key Results

Intimate synorganisation of floral organs is effected by the formation of five separate nectar canals for the proboscis of pollinators. Each nectar canal is formed by six adjacent organs from four organ whorls. In addition, the sepals are hooked together by the formation of longitudinal ribs and grooves, and provide a firm scaffold for the canals. Obdiplostemony provides a guide rail within each canal formed by the flanks of the antepetalous stamen filaments.

Conclusions

Intimate synorganisation in flowers can be realized without any fusion, and obdiplostemony may play a role in this synorganisation.     

Ultrastructural changes in skeletal muscle of the tail of the lizard Hemidactylus mabouia immediately following autotomy

Araújo, T.H., Faria, F.P., Katchburian, E. and Freymüller, E. (2009). Ultrastructural changes in skeletal muscle of the tail of the lizard Hemidactylus mabouia immediately following autotomy. —Acta Zoologica (Stockholm) 91 : 440–446. Although autotomy and subsequent regeneration of lizard tails has been extensively studied, there is little information available on ultrastructural changes that occur to the muscle fibers at the site of severance. Thus, in the present study, we examine the ultrastructure of the musculature of the remaining tail stump of the lizard Hemidactylus mabouia immediately after autotomy. Our results show that exposed portions of the skeletal muscle fibers of the stump that are unprotected by connective tissue bulge to produce large mushroom‐like protrusions. These exposed portions show abnormal structure but suffer no leakage of cytoplasmic contents. Many small and large vesicular structures appeared between myofibrils in the interface at this disarranged region (distal) and the other portion of the fibers that remain unchanged (proximal). These vesicles coalesce, creating a gap that leads to the release of the mushroom‐like protrusion. So, our results showed that after the macroscopic act of autotomy the muscular fibers release part of the sarcoplasm as if a second and microscopic set of autotomic events takes place immediately following the macroscopic act of autotomy. Presumably these changes pave the way for the formation of a blastema and the beginning of regeneration.