Seasonality, microhabitat and cryptic variation in tropical salamander reproductive cycles

In many salamanders, most aspects of reproduction coincide with seasonal changes in abiotic factors such as temperature and humidity. However, while these reproductive patterns have been well documented for temperate salamanders, detailed data for tropical species are relatively sparse. I used histological techniques to examine temporal variation in the spermatogenetic cycles of four species of Guatemalan bolitoglossine salamanders ( Bolitoglossa occidentalis , B. rostrata , Dendrotriton bromeliacia and Pseudoeurycea goebeli ) from different microhabitats along an elevational gradient. All four species have mature sperm present in the testis throughout the year, irrespective of patterns of courtship and egg-laying. Additionally, the two species from more seasonal habitats ( B. occidentalis and B. rostrata ) exhibit significant but cryptic levels of variation in the amount of spermatozoa present in the testis not detectable by external appearance or the presence of secondary sexual characteristics. For the two species from less seasonal cloud forests ( D. bromeliacia and P. goebeli ), there were no detectable patterns to variation within the testis. Regional variation in climate undoubtedly influences reproductive cycles, however, microhabitat and the immediate environment are also important determinants of reproductive strategy.  © 2003 The Linnean Society of London . Biological Journal of the Linnean Society , 2003, 78 , 489–496.     

Controls over reproductive phenology among ungulates: allometry and tropical‐temperate contrasts

Ungulates inhabiting high latitudes schedule the timing of conceptions so that offspring are born during the most favourable nutritional conditions for reproductive success. The optimal period for births is less reliably predictable in tropical and subtropical savanna environments where plant growth is governed by rainfall, suggesting that reproductive phenology could be influenced more proximately by resources affecting the body condition of females around the time of conceptions. To assess how these controls operate, we compared the timing of births and conceptions among tropical and subtropical savanna ungulates with the patterns shown by ungulates in northern temperate or subarctic latitudes. The association between the timing of births and the onset of plant growth early in the growing season is less consistent among tropical savanna ungulates than among ungulates inhabiting northern temperate environments, and apparently subject to other influences affecting vegetation phenology. Nevertheless, birth peaks seem to coincide with the time of the year when forage quality is expected to be best for offspring survival and growth for most tropical or subtropical ungulates with gestation periods shorter than a year. When gestation time exceeds one year, proximal effects of nutritional conditions around the time of conceptions apparently become overriding and birth synchrony with early season plant growth is no longer effective. Proximate nutritional influences on conceptions may also govern the somewhat diffuse spread of births shown by ungulate populations in equatorial latitudes where photoperiod cues controlling oestrus and mating cannot be used to schedule the later timing of births.     

Age Determination of Frogs and Toads (Amphibia, Anura) from North-western Europe

Age was determined in three anuran species inhabiting a temperate oceanic climate ( Rana temporaria, Bufo calamita and Bufo bufo ) by means of the histological structure of the phalanges. Narrow, haematoxylinophilic lines were visible in these, and evidence from the examination of subadults and frog ( R. temporaria ) recaptures showed the lines to be annual. The validity of using the lines as age indicators was tested most extensively on natural frog populations and the effects of endosteal resorption were not found to be significant. The evidence for this conclusion was provided directly by recapture data and indirectly by an analysis of histological measurements made on the phalanges.     

Temperature and humidity alter prolactin receptor expression in the skin of toad (Bufo bankorensis and Bufo melanostictus)

Bufo bankorensis and Bufo melanostictus, the only two species of Bufonidae genus in Taiwan, live in habitats that differ in altitude and humidity. This study tested the hypothesis that prolactin receptor (PRLR) expression responds to environmental change. Western blot analysis showed that the PRLR protein was widely distributed in brain, lung, liver, kidney, dorsal skin and ventral skin of toads. The level PRLR protein was elevated in the dorsal skin of the two toad species treated with dry or wet conditions for 14 days. The increase in PRLR of dorsal skin in B. bankorensis was higher than that in B. melanostictus. This experimental result suggests that B. bankorensis secretes more mucus to reduce water evaporation from its thinner cuticle than B. melanostictus. The expression of PRLR protein was increased in the lung of B. bankorensis and decreased in the lung of B. melanostictus. Moreover, PRLR protein levels were increased in the kidneys in the two species toad, likely due to reduction in water lost through lung and urine. The two toad species were subjected to varying temperatures (25 degrees C, 15 degrees C and 10 degrees C) for 14 days. The lowest PRLR protein expression was observed at 10 degrees C. Comparison of the decreasing trend in PRLR protein levels demonstrated that the variation in B. bankorensis was significantly higher than that in B. melanostictus. Comparisons of variation in PRLR protein expression in the two species under different environments suggest that B. bankorensis is more adaptable to different environments than B. melanostictus.     

Postponed reproduction as an adaptation to winter conditions in Drosophila melanogaster: evidence for clinal variation under semi-natural conditions

Patterns of climatic adaptation in drosophila and other insects have largely been inferred from laboratory comparisons of traits that vary clinally. Here, we extend this research to comparisons under semi-natural conditions. To test for clinal variation in reproductive patterns and survival over winter, Drosophila melanogaster populations were initiated from seven collection sites along the eastern coast of Australia, ranging from tropical to temperate regions. The fecundity and survival of these populations were monitored in field cages at a temperate location until all adults had died more than 5 months later. Total fecundity showed a curvilinear relationship with latitude, due to higher egg production by high- and low-latitude populations. Adults from temperate locations survived winter conditions better than those from subtropical populations but not tropical ones. There was a linear cline in the timing of egg production: temperate populations produced eggs later than populations from lower latitudes. This cline is likely to be adaptive because egg-to-adult viability experiments indicated that only eggs laid in spring developed successfully to the adult stage. There was no evidence for climatic adaptation in the immature stages. The adult mortality rate increased gradually over winter, and in some populations was also correlated with the minimum ambient temperature. These results indicate that adaptation to winter conditions in D. melanogaster has involved shifts in reproductive patterns.     

Potential refugia in Taiwan revealed by the phylogeographical study of Castanopsis carlesii Hayata (Fagaceae)

In this study, we examined spatial patterns of chloroplast DNA (cpDNA) variation in a total of 30 populations of Castanopsis carlesii Hayata (Fagaceae), a subtropical and temperate tree species, including 201 individuals sampled throughout Taiwan. By sequencing two cpDNA fragments using universal primers (the trnL intron and the trnV-trnM intergenic spacer), we found a total of 1663 bp and 21 polymorphic sites. These gave rise to a total of 28 cpDNA haplotypes. The level of differentiation among the populations studied was relatively high (GST = 0.723). Two ancestral haplotypes are widely distributed. The Central Mountain Ridge (CMR) of Taiwan represents an insurmountable barrier to the east-west gene flow of C. carlesii. Among the populations studied, three separated populations, at Lienhuachih, Fushan and Lichia, have high nucleotide diversity. Estimates of NST-GST for populations on both sides of the CMR indicate that no phylogeographical structure exists. According to the genealogical tree, number of rare haplotype and population genetic divergence, this study suggests that two potential refugia existed during the last glaciation: the first refugium was located in a region to the north of Hsuehshan Range (HR) and west of the CMR; the second refugium was located in south, especially southeastern Taiwan. In fact, the second refugium happens to be the same as that reported for Quercus glauca. A 'star-like' genealogy is characteristic when all haplotypes rapidly coalesce and is a general outcome of population expansion. The neutrality test and mismatch distribution also suggest demographic expansion recovering from a bottleneck.     

Biological traits and growth patterns of pejerrey Odontesthes argentinensis

This study assesses for the first time the relationship between annual cycles of different biological indices with growth patterns of a marine pejerrey Odontesthes argentinensis population near its southern‐distribution boundary in North Patagonia. The reproductive period is between September and November evidenced by an increase in the gonado‐somatic index with a peak in October corresponding to spawning. The reproductive cycle was also coupled with metabolic processes related to energy allocation as shown by changes in the hepato‐somatic index and body condition. Total length (L_T) at maturity was 270 for females and 282 mm for males, whereas fecundity was estimated at mean ±s.d . = 9380 ± 1797 mature oocytes. Based on the marginal increment analysis, most of the scales showed a maximum value during summer, with a sharp decline thereafter during autumn and winter, indicating that scale rings are formed during the latter period and only once a year. Growth fitted by the von Bertalanffy model for both males and females did not show significant differences and showed a rapid growth during the first 2 years. The shorter reproductive period compared with that of the northern O. argentinensis populations inhabiting tropical and subtropical areas was interpreted as an adjustment to temperate environmental conditions. The larger maximum L_T and L_T at first maturity are in agreement with the counter‐gradient hypothesis and could be related to the selective effects of low temperature and a shorter growing season. This latitude dependency argues strongly against the application of the same fishing regulations for different O. argentinensis populations as a whole and reinforces the need to assess basic biological features at a population scale to promote local sustainable fisheries management.     

Temperature tolerance of the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae) in tropical and temperate regions of Asia

Temperature tolerance was investigated in nine populations of Plutella xylostella Linnaeus from tropical and temperate regions of Asia. At all rearing temperatures between 15 and 35 degrees C, no clear differences were observed in female egg production or larval development between tropical and temperate populations. Thus, tropical populations did not show a high-temperature tolerance superior to that of the temperate populations. In all populations, the net reproductive rate (number of new females born per female) largely depended on the number of eggs laid per female, and egg production significantly decreased with increasing temperature (P < 0.001). Larval developmental rate also showed a significant positive correlation with temperature (P < 0.001). Per cent hatch of eggs and larval survival did not show a significant correlation with temperature: hatching was constant between 15 and 32.5 degrees C, but considerably lower at 35 degrees C. Larval survival was similar between 15 and 30 degrees C, appreciably lower at 32.5 degrees C and declined to 0% at 35 degrees C. Based on these results, environmental conditions under which P. xylostella can maintain a high population density throughout the year in tropical and subtropical regions are discussed.     

Phylogeny of east asian bufonids inferred from mitochondrial DNA sequences (Anura: amphibia)

We investigated the relationships of Asian bufonids using partial sequences of mitochondrial DNA genes. Twenty-six samples representing 14 species of Bufo from China and Vietnam and 2 species of Torrentophryne from China were examined. Three samples of Bufo viridis from Armenia and Georgia were also sequenced to make a comparison to its sibling tetraploid species B. danatensis. Bufo americanus, from Canada, was used as the outgroup. Sequences from the 12S ribosomal RNA, 16S ribosomal RNA, cytochrome b, and the control region were analyzed using parsimony. East Asian bufonids were grouped into two major clades. One clade included B. andrewsi, B. bankorensis, B. gargarizans, B. tibetanus, B. tuberculatus, its sister clade B. cryptotympanicus, and the 2 species of Torrentophryne. The second clade consisted of B. galeatus, B. himalayanus, B. melanostictus, and a new species from Vietnam. The placement of three taxa (B. raddei, B. viridis, and its sister species, B. danatensis) was problematic. The genus Torrentophryne should be synonymized with Bufo to remove paraphyly. Because B. raddei does not belong to the clade that includes B. viridis and B. danatensis, it was removed from the viridis species group. The species status of B. bankorensis from Taiwan is evaluated.     

Implications of climate change for the reproductive capacity and survival of New World silversides (family Atherinopsidae)

The New World silversides (family Atherinopsidae) are found in marine, estuarine and inland waters of North, Central and South America, where they are ecologically important as forage fishes and sometimes economically important for commercial and recreational fisheries. This report reviews the knowledge of the reproductive attributes of temperate and subtropical atherinopsids in relation to temperature and discusses the potential effects of climate change on their reproduction and adaptive responses. Their reproductive cycles are primarily entrained by photoperiod with high temperature acting as a limiting factor. They are generally multiple spawners which release successive batches of eggs in spring, but some species can spawn also in autumn and even summer when temperatures do not increase excessively. The decoupling of temperature patterns and photoperiod with further global warming and associated asymmetric thermal fluctuations could lead to spawning at times or temperatures that are unsuitable for larval development and growth. Many members of this family show temperature-dependent sex determination (TSD), where the phenotypic sex of an individual is determined partly or wholly by the temperature experienced during gonadal sex differentiation, and high-temperature induced germ cell degeneration and decreased fertility. The predicted short-term reproductive responses of atherinopsids to climate change therefore include acceleration, shortening or overall disruption of spawning activity, and also more subtle, but nonetheless equally population-threatening, dysfunctions such as highly skewed sex ratios and partial or total loss of fertility. In the case of species with TSD, asymmetric thermal fluctuations could also cause larvae to encounter temperatures lower than normal during early development and be feminized. Such dysfunctions have been documented already in natural populations but are confined so far to landlocked, inland water habitats, perhaps because they impose more severe thermal fluctuations and limitations to migration and dispersal. The severity and recurrence of these dysfunctions with further climate change will depend both on the magnitude, speed and pattern of change and on how much (or how fast) physiological and behavioural traits can evolve to match the new conditions imposed by the climate, which is largely unknown. In this regard, compelling evidence is shown that numerous traits, including the sex determination system, are capable of rapid evolution and could mitigate the negative effects of temperature increases on population viability in atherinopsids.     

A comparison of energy substrates and reproductive patterns of two anurans. Acris crepitans and Bufo woodhousei

The seasonal pattern of carcass, liver and ovary lipid and liver non-lipid mass was examined in the cricket frog, Acris crepitans, and Woodhouse's toad, Bufo woodhousei. Reproductive patterns were also studied. The over-winter reduction of body lipid and liver non-lipid material was attributed to metabolism in Acris crepitans. Male, but not female, Bufo woodhousei exhibited seasonal variation in lipid stores that was attributable to metabolism. Females, but not males, showed seasonal variation in liver non-lipid mass and quantified liver glycogen. Females of both species mobilized body lipid during the period of ovarian development; however, an inverse relationship between fatbody mass and ovary mass was evident for Acris, only. Female Acris crepitans depleted all ovarian follicles prior to brumation; however, Bufo woodhousei retained enlarged follicles throughout the year. Variation in metabolic substrate use between species was related to the differences in reproductive patterns exhibited by the two anurans. These variations in reproductive strategy represent adaptations that enhance the survivability of different species in dissimilar habitats.     

Additional Records of Trematodes of Amphibians and Reptiles from Taiwan

Three monogenetic and 23 digenetic trematodes of amphibians and reptiles are reported from Taiwan, 14 for the first time. One new family and genus and five new species of Digenea are described: Omphalometridae, Leurosoma taiwanense sp.n. from Bufo bufo bankorensis; Dicrocoeliidae, Paradistomum taiwanense sp.n. from Natrix stolata; Ocadiatrematidae, Ocadiatrema taiwanense fam. gen. et sp.n. from Ocadia sinensis; Lecithodendriidae, Prosthodendrium (Paralecithodendrium)taiwanense sp.n. from Ocadia sinensis; Pleurogenidae, Nenimandijea taiwanense sp.n. from Rana plancyi fukienensis .     

Resource availability and roosting ecology shape reproductive phenology of rain forest insectivorous bats

Bats in temperate and subtropical regions typically synchronize birth of a single young with peaks in resource availability driven by local climate patterns. In tropical rain forest, insects are available throughout the year, potentially allowing departures from seasonal monoestry. However, reproductive energy budgets may be constrained by the cost of commuting to foraging grounds from distant roosts. To test these hypotheses, we simultaneously tracked female reproductive activity of 11 insectivorous bat species, insect biomass, and local weather variables for 20 months in a Malaysian rain forest. Five species roost in forest structures and hence have low commuting costs, whereas six species depend on caves, which are limited in the landscape, and are presumed to incur higher commuting costs to foraging sites. Monthly insect biomass was positively correlated with monthly rainfall, and there was a significant relationship between insect biomass and lactation in cave‐roosting but not forest‐roosting species. Cave‐roosting species were seasonally monoestrus, with parturition confined to a two‐month period, whereas in forest‐roosting species, pregnancy and lactation were recorded throughout the year. Our results suggest that the energetic costs of commuting from roosts to foraging grounds shape annual reproductive patterns in tropical rain forest insectivorous bats. Ongoing changes in forest landscapes are likely to increase these costs for cave‐roosting bats, further restricting reproductive opportunities. Climate change is projected to influence the timing of rainfall events in many tropical habitats, which may disrupt relationships between rainfall, insect biomass, and bat reproductive timing, further compromising reproductive success.     

Metabolic and ventilatory responses to hypoxia in two altitudinal populations of the toad, Bufo bankorensis

Effects of hypoxia on resting oxygen consumption (MO2), lung ventilation, and heart rate at different ambient PO2 were compared between lowland and high altitude populations of the toad, Bufo bankorensis. Resting MO2 decreased significantly in mild hypoxia (PO2 = 120 mm Hg) at 10 degrees C and in moderate hypoxia (PO2 = 80 mm Hg) at 25 degrees C in both altitudinal populations; however, resting MO2 did not differ significantly between the two populations. Numbers of lung ventilation periods (VP) and total inspired volume (VL) did not change with PO2 at 10 degrees C, but did increase at moderate and severe hypoxia (40 mm Hg), respectively, at 25 degrees C. Resting heart rates did not change during hypoxia and did not differ between altitude populations. The results suggest (1) the effect of PO2 change on MO2 should be considered in future studies involving transfer of anurans to a different altitude; and (2) the metabolic and ventilatory physiology in B. bankorensis does not compensate for the low temperature and PO2 at high altitude.     

Lineage-specific late pleistocene expansion of an endemic subtropical gossamer-wing damselfly, Euphaea formosa, in Taiwan

Background  

Pleistocene glacial oscillations have significantly affected the historical population dynamics of temperate taxa. However, the general effects of recent climatic changes on the evolutionary history and genetic structure of extant subtropical species remain poorly understood. In the present study, phylogeographic and historical demographic analyses based on mitochondrial and nuclear DNA sequences were used. The aim was to investigate whether Pleistocene climatic cycles, paleo-drainages or mountain vicariance of Taiwan shaped the evolutionary diversification of a subtropical gossamer-wing damselfly, Euphaea formosa.     

Flowering and Fruiting Patterns in a Subtropical Rain Forest,Taiwan

Reproductive patterns of tropical and temperate plants are usually associated with climatic seasonality, such as rainfall or temperature, and with their phylogeny. It is still unclear, however, whether plant reproductive phenology is influenced by climatic factors and/or phylogeny in aseasonal subtropical regions. The plant reproductive phenology of a subtropical rain forest in northern Taiwan (24°45′ N, 121°35′ E) was monitored at weekly intervals during a 7‐yr period (2002–2009). The flowering patterns of 46 taxa and fruiting patterns of 26 taxa were examined and evaluated in relation to climatic seasonality, phylogenetic constraints, and different phenophases. Our results indicated that most of the studied species reproduced annually. Additionally, both community‐wide flowering and fruiting patterns exhibited distinct annual rhythms and varied little among years. The community flowering peak matched seasonal changes in day length, temperature, and irradiance; while the community fruiting peak coincided with an increase in bird richness and the diet‐switching of resident omnivorous birds. In addition, phylogenetically closely related species tended to reproduce during the same periods of a year. Neither the mean flowering dates nor seasonal variation in solar radiation, however, was related to the fruit development times. Our results indicate the importance of abiotic, biotic, and evolutionary factors in determining the reproductive phenology in this subtropical forest.     

Overwintering in Drosophila melanogaster: outdoor field cage experiments on clinal and laboratory selected populations help to elucidate traits under selection

Insects can adapt to temperate environments by increasing levels of resistance to cold conditions over winter and/or altering reproductive patterns to focus reproduction in favourable conditions. In temperate areas, Drosophila melanogaster persists over winter at the adult stage. A previous experiment, conducted with flies kept in outdoor population cages in the temperate winter, indicated that temperate populations produced more eggs than did tropical populations following an abrupt increase in reproduction in late winter. In contrast, the tropical populations produced more eggs prior to the increase. Both patterns resulted in a higher net number of surviving offspring for temperate populations. Here we again examine the clinal pattern in reproduction using outdoor cages, this time held under tropical winter conditions. In this environment, surprisingly, egg production was higher and on average earlier in populations originating from temperate areas. However, mortality rates also increased with latitude of origin, and the relationship of lifetime egg production to latitude should therefore be measured. To test the role of altered pattern of egg production per se in the reproductive advantage of temperate populations in the temperate winter, we tested the performance of laboratory lines selected for altered reproductive patterns, under temperate winter conditions. Lines selected for high early fecundity exhibited this characteristic in the field cages and lines selected for late reproduction exhibited a relatively high fecundity in spring. The timing of the abrupt increase in egg production was identical in these sets of lines and occurred at the same time in recently collected populations, suggesting evolutionary conservation of the switch. These findings suggest that changes in early and late reproduction per se determine adaptation to temperate winter conditions, and illustrate how laboratory selection lines can be used to understand traits underlying adaptive shifts in field performance.     

Potential ‘costs of reproduction’ in a skink: Inter‐ and intrapopulational variation

Reproductive costs are important determinants of reproductive effort in squamate reptiles. Consequently, differences in costs of reproduction between populations of geographically or climatically widespread species are likely to result in different patterns of reproductive effort. In the present study, the effect of pregnancy on sprint speed was examined in a small viviparous skink, Niveoscincus ocellatus (Gray 1845), from two populations at the climatic extremes of its distribution. Decreased sprint speed has the potential to be an important cost of reproduction in this species, through a reduced ability to avoid predation and/or decreased foraging efficiency. Lizards inhabiting the colder site were larger than those from the warmer site and, contrary to predictions from life history theory, had a higher reproductive effort. In both populations, sprint speed was lower in pregnant lizards than in either the same individuals after birth or non‐pregnant control lizards. Within each population, sprint speed was unrelated to the level of reproductive effort of the female in terms of either absolute mass of the reproductive burden or the burden relative to her post‐partum body mass. However, within each population, the mass of the clutch that an individual female was carrying relative to snout–vent length was an important determinant of her sprint speed while pregnant. Thus, within each population, a relatively high reproductive burden may potentially increase costs of reproduction in this species. Despite this relationship and predictions from life history theory suggesting that annual reproductive effort will be lower in populations with a large body size and delayed maturity, it is suggested that a higher reproductive effort at the cold site is possible because they have a higher absolute sprint speed because of their larger size and a relatively higher abundance of cover at the cold site, and differences in predation pressure may alter selective pressures on reproductive investment.     

The island syndrome in isolated populations of a tropical forest rodent

I examined population traits of eight isolated populations of a tropical forest rodent (Proechimys semispinosus, the Central American spiny rat) for 1 year in central Panamá. Populations were sampled by monthly live-trapping, and seven traits (density, population growth rate, adult survival, reproductive effort, age structure, sex ratio, and body mass) were compared among populations. I also compared results with published data from nearby mainland populations. Each isolated population showed characteristics typical of island populations when compared with mainland populations, including higher and more stable densities, reduced reproductive effort, and greater body mass. Densities were the highest yet recorded for this species, and biomass of these island populations was among the highest of any tropical rodent yet studied. Population traits varied not only between island and mainland populations but also among island populations. P. semispinosus have traits that allow individuals in a population to rapidly respond to temporal changes in habitat quality or resource abundance. These traits include a high reproductive rate and an ability to adjust reproductive effort to changes in density. P. semispinosus are therefore able to quickly reach and maintain high densities under favorable conditions, thereby allowing close tracking of temporally and spatially varying resources. This flexibility is predicted for habitat generalists and presumably promotes abundance and persistence in temporally and spatially heterogeneous environments. P. semispinosus, often the most abundant and widely distributed species of rodent in forests throughout their geographic range, therefore have traits that are similar to those of generalist rodents in temperate forests.     

Population history and genetic structure of a circumpolar species: the arctic fox

The circumpolar arctic fox Alopex lagopus thrives in cold climates and has a high migration rate involving long-distance movements. Thus, it differs from many temperate taxa that were subjected to cyclical restriction in glacial refugia during the Ice Ages. We investigated population history and genetic structure through mitochondrial control region variation in 191 arctic foxes from throughout the arctic. Several haplotypes had a Holarctic distribution and no phylogeographical structure was found. Furthermore, there was no difference in haplotype diversity between populations inhabiting previously glaciated and unglaciated regions. This suggests current gene flow among the studied populations, with the exception of those in Iceland, which is surrounded by year-round open water. Arctic foxes have often been separated into two ecotypes: 'lemming' and 'coastal'. An analysis of molecular variance suggested particularly high gene flow among populations of the 'lemming' ecotype. This could be explained by their higher migration rate and reduced fitness in migrants between ecotypes. A mismatch analysis indicated a sudden expansion in population size around 118 000 BP, which coincides with the last interglacial. We propose that glacial cycles affected the arctic fox in a way opposite to their effect on temperate species, with interglacials leading to short-term isolation in northern refugia.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 79–89.