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Life histories and conservation of long-lived reptiles, an illustration with the American crocodile (Crocodylus acutus)

Successful species conservation is dependent on adequate estimates of population dynamics, but age-specific demographics are generally lacking for many long-lived iteroparous species such as large reptiles. Accurate demographic information allows estimation of population growth rate, as well as projection of future population sizes and quantitative analyses of fitness trade-offs involved in the evolution of life-history strategies. Here, a long-term capture–recapture study was conducted from 1978 to 2014 on the American crocodile ( Crocodylus acutus ) in southern Florida. Over the study period, 7,427 hatchlings were marked and 380 individuals were recaptured for as many as 25 years. We estimated survival to be strongly age dependent with hatchlings having the lowest survival rates (16%) but increasing to nearly 90% at adulthood based on mark–recapture models. More than 5% of the female population were predicted to be reproductive by age 8 years; the age-specific proportion of reproductive females steadily increased until age 18 when more than 95% of females were predicted to be reproductive. Population growth rate, estimated from a Leslie–Lefkovitch stage-class model, showed a positive annual growth rate of 4% over the study period. Using a prospective sensitivity analysis, we revealed that the adult stage, as expected, was the most critical stage for population growth rate; however, the survival of younger crocodiles before they became reproductive also had a surprisingly high elasticity. We found that variation in age-specific fecundity has very limited impact on population growth rate in American crocodiles. We used a comparative approach to show that the original life-history strategy of American crocodiles is actually shared by other large, long-lived reptiles: while adult survival rates always have a large impact on population growth, this decreases with declining increasing growth rates, in favour of a higher elasticity of the juvenile stage. Crocodiles, as a long-lived and highly fecund species, deviate from the usual association of life histories of “slow” species. Current management practices are focused on nests and hatchling survival; however, protection efforts that extend to juvenile crocodiles would be most effective for conservation of the species, especially in an ever-developing landscape.

Journal of Animal Ecology↗

Osmoregulatory physiology and rapid evolution of salinity tolerance in threespine stickleback recently introduced to fresh water

Background: Post-Pleistocene diversification of threespine stickleback in fresh water offers a valuable opportunity to study how changes in environmental salinity shape physiological evolution in fish. In Alaska, the presence of both ancestral oceanic populations and derived landlocked populations, including recent lake introductions, allows us to examine rates and direction of evolution of osmoregulation following halohabitat transition. Hypotheses: Strong selection for enhanced freshwater tolerance will improve survival of recently lake-introduced stickleback in ion-poor conditions compared with their oceanic ancestors. Trade-offs between osmoregulation in fresh water and seawater will allow members of the ancestral population to survive better in response to seawater challenge, as mediated by upregulating salt-secreting transporters in the gill. Poorer hypo-osmoregulatory performance of derived fish will be marked by higher levels of taurine and other organic osmolytes. Methods: We reared clutches at a common salinity from an anadromous and a descendant population, Scout Lake, which has been landlocked for only two generations. We challenged 6-week-old juveniles with extreme low and high salinity treatments and sampled fish over 10 days to investigate putative molecular mechanisms underlying differences in halotolerance. We measured whole-body organic osmolyte content as well as gill Na + /K + -ATPase (NKA) activity and Na + /K + /2Cl − cotransporter (NKCC) protein abundance. Other juveniles from these populations and also from Cheney Lake, a fourth-generation landlocked descendant, were gradually salt-acclimated to determine maximum halotolerance limits. Results: Scout Lake stickleback exhibited 67% higher survival in fresh water than the ancestral anadromous population, but individuals from both groups exhibited similar seawater tolerance. Likewise, the gradual salinity threshold for each population was equivalent (71 ppt). Gill NKA activity and NKCC abundance were both higher in seawater-challenged fish, but did not differ between populations. Sticklebacks from both populations responded to acute salinity stress by transiently increasing osmolyte levels in seawater and decreasing them in fresh water. Conclusion: Enhanced freshwater tolerance has evolved rapidly in recently landlocked stickleback compared with their anadromous ancestors (0.569 haldanes), but the former have retained ancestral seawater-osmoregulatory function.

Evolutionary Ecology Research↗

Demography, environmental uncertainty, and the evolution of mate desertion in the snail kite

The Snail Kite (Rostrhamus sociabilis), an endangered hawk, has a unique mating system in Florida (Beissinger and Snyder 1987): when food is abundant, males or females desert their mates at nearly equal frequency (ambisexual mate desertion) in the midst of a nesting cycle. I examined the demographic and environmental constraints selecting for a clutch size that permits one parent to desert, yet optimizes the number of offspring produced by each parent. Demographic studies, conducted from 1979—1983, indicated that kites have (1) a very high nest failure rate (° = 68%) due most often to unstable nest sites and predation, (2) a variable nesting season (5—10 mo/yr), (3) an early age of first reproduction for a bird this size (10 mo), (4) a high degree of iteroparity (double and potentially triple clutching within a season), and (5) unstable populations. Both nesting success and population size were directly related to Everglades water levels and resultant snail densities. Kites responded to large annual changes in food abundance, not by adjusting clutch size but by deserting their mates and presumably attempting to renest. Kite demographic traits appear to be adaptations to or results of an uncertain environment. Based on 67 yr of Everglades water levels, environmental predictability, measured by spectral analysis and Colwell's (1974) index, was low and influenced by water management regimes: (1) water levels were lowered, (2) annual variation in levels increased and annual cycles became stronger, (3) the period length of long—term drought—flood cycles shifted from 10 or more yr toward 5 yr, and (4) levels became a less predictive cue for favorable nesting conditions. A potential evolutionary pathway from biparental care to mate desertion in Snail Kites is proposed. It is unlikely that mate desertion evolved solely from a context of conflict between the sexes, because kite nesting success is so low that it is probably maladaptive for a parent to desert and jeopardize the survival of any of its first brood. Instead, mate desertion behavior probably evolved in response to a smaller average clutch size; this would allow females to be highly iteroparous and avoid the costs of overinvestment, and should be strongly favored in a highly uncertain environment. Analysis of clutches in museum collections suggests that an apparent decline in clutch size may have occurred in Florida during the past century. The potential for ambisexual mate desertion to occur in other vertebrates is during the past century. The potential for ambisexual mate desertion to occur in other vertebrates is examined.

Ecology↗

Integrative phylogenetic, phylogeographic and morphological characterisation of the Unio crassus species complex reveals cryptic diversity with important conservation implications

The global decline of freshwater mussels and their crucial ecological services highlight the need to understand their phylogeny, phylogeography and patterns of genetic diversity to guide conservation efforts. Such knowledge is urgently needed for Unio crassus , a highly imperilled species originally widespread throughout Europe and southwest Asia. Recent studies have resurrected several species from synonymy based on mitochondrial data, revealing U. crassus to be a complex of cryptic species. To address long-standing taxonomic uncertainties hindering effective conservation, we integrate morphometric, phylogenetic, and phylogeographic analyses to examine species diversity within the U. crassus complex across its entire range. Phylogenetic analyses were performed using cytochrome c oxidase subunit I (815 specimens from 182 populations) and, for selected specimens, whole mitogenome sequences and Anchored Hybrid Enrichment (AHE) data on ∼600 nuclear loci. Mito-nuclear discordance was detected, consistent with mitochondrial DNA gene flow between some species during the Pliocene and Pleistocene. Fossil-calibrated phylogenies based on AHE data support a Mediterranean origin for the U. crassus complex in the Early Miocene. The results of our integrative approach support 12 species in the group: the previously recognised Unio bruguierianus , Unio carneus, Unio crassus , Unio damascensis , Unio ionicus , Unio sesirmensis , and Unio tumidiformis , and the reinstatement of five nominal taxa: Unio desectus stat. rev. , Unio gontierii stat. rev. , Unio mardinensis stat. rev. , Unio nanus stat. rev. , and Unio vicarius stat. rev. Morphometric analyses of shell contours reveal important morphospace overlaps among these species, highlighting cryptic, but geographically structured, diversity. The distribution, taxonomy, phylogeography, and conservation of each species are succinctly described.

Molecular Phylogenetics and Evolution↗

Enclosed nests may provide greater thermal than nest predation benefits compared with open nests across latitudes

Nest structure is thought to provide benefits that have fitness consequences for several taxa. Traditionally, reduced nest predation has been considered the primary benefit underlying evolution of nest structure, whereas thermal benefits have been considered a secondary or even non-existent factor. Yet, the relative roles of these factors on nest structures remain largely unexplored. Enclosed nests have a constructed or natural roof connected to sides that allow a restricted opening or tube entrance that provides cover in all directions except the entrance, whereas open nests are cups or platforms that are open above. We show that construction of enclosed nests is more common among songbirds (Passeriformes) in tropical and southern hemisphere regions than in north temperate regions. This geographic pattern may reflect selection from predation risk, under long-standing assumptions that nest predation rates are higher in southern regions and that enclosed nests reduce predation risk compared with open cup nests. We therefore compared nest predation rates between enclosed vs. open nests in 114 songbird species that do not nest in tree holes among five communities of coexisting birds, and for 205 non-hole-nesting species from the literature, across northern temperate, tropical, and southern hemisphere regions. Among coexisting species, enclosed nests had lower nest predation rates than open nests in two south temperate sites, but not in either of two tropical sites or a north temperate site. Nest predation did not differ between nest types at any latitude based on literature data. Among 319 species from both our field studies and the literature, enclosed nests did not show consistent benefits of reduced predation and, in fact, predation was not consistently higher in the tropics, contrary to long-standing perspectives. Thermal benefits of enclosed nests were indicated based on three indirect results. First, species that built enclosed nests were smaller than species using open nests both among coexisting species and among species from the literature. Smaller species lose heat fastest and thereby may gain important thermal benefits from reduced convective cooling. Second, eggs were warmed by parents for less time in species with enclosed nests, as can be expected if egg cooling rates are slower. Finally, species using enclosed nests exhibited enhanced growth of mass and wings compared with species using open nests, suggesting reduced thermoregulatory costs allowed increased energy for growth. Enclosed nests may therefore provide more consistent thermal than nest predation benefits, counter to long-standing perspectives.

Functional Ecology↗