Sequestered defensive toxins in tetrapod vertebrates: principles, patterns, and prospects for future studies

Chemical defenses are widespread among animals, and the compounds involved may be either synthesized from nontoxic precursors or sequestered from an environmental source. Defensive sequestration has been studied extensively among invertebrates, but relatively few examples have been documented among vertebrates. Nonetheless, the number of described cases of defensive sequestration in tetrapod vertebrates has increased recently and includes diverse lineages of amphibians and reptiles (including birds). The best-known examples involve poison frogs, but other examples include natricine snakes that sequester toxins from amphibians and two genera of insectivorous birds. Commonalities among these diverse taxa include the combination of consuming toxic prey and exhibiting some form of passive defense, such as aposematism, mimicry, or presumptive death-feigning. Some species exhibit passive sequestration, in which dietary toxins simply require an extended period of time to clear from the tissues, whereas other taxa exhibit morphological or physiological specializations that enhance the uptake, storage, and/or delivery of exogenous toxins. It remains uncertain whether any sequestered toxins of tetrapods bioaccumulate across multiple trophic levels, but multitrophic accumulation seems especially likely in cases involving consumption of phytophagous or mycophagous invertebrates and perhaps consumption of poison frogs by snakes. We predict that additional examples of defensive toxin sequestration in amphibians and reptiles will be revealed by collaborations between field biologists and natural product chemists. Candidates for future investigation include specialized predators on mites, social insects, slugs, and toxic amphibians. Comprehensive studies of the ecological, evolutionary, behavioral, and regulatory aspects of sequestration will require teams of ecologists, systematists, ethologists, physiologists, molecular biologists, and chemists. The widespread occurrence of sequestered defenses has important implications for the ecology, evolution, and conservation of amphibians and reptiles.     

Ecological determinism increases with organism size

After much debate, there is an emerging consensus that the composition of many ecological communities is determined both by species traits, as proposed by niche theory, as well as by chance events. A critical question for ecology is, therefore, which attributes of species predict the dominance of deterministic or stochastic processes. We outline two hypotheses by which organism size could determine which processes structure ecological communities, and we test these hypotheses by comparing the community structure in bromeliad phytotelmata of three groups of organisms (bacteria, zooplankton, and macroinvertebrates) that encompass a 10 000-fold gradient in body size, but live in the same habitat. Bacteria had no habitat associations, as would be expected from trait-neutral stochastic processes, but still showed exclusion among species pairs, as would be expected from niche-based processes. Macroinvertebrates had strong habitat and species associations, indicating niche-based processes. Zooplankton, with body size between bacteria and macroinvertebrates, showed intermediate habitat associations. We concluded that a key niche process, habitat filtering, strengthened with organism size, possibly because larger organisms are both less plastic in their fundamental niches and more able to be selective in dispersal. These results suggest that the relative importance of deterministic and stochastic processes may be predictable from organism size.     

Underlying causes of habitat-associated differences in size of age-0 walleye pollock (Theragra chalcogramma) in the Gulf of Alaska

Age-0 walleye pollock (Theragra chalcogramma) caught in September in the Gulf of Alaska display habitat-associated differences in standard length (SL). Age-0 fish collected in the region around Sutwik Island and 375?km farther downstream near the Shumagin Islands most likely originate from the Shelikof Strait spawning aggregation. However, age-0 fish resulting from the same spawning aggregation differ in mean size up to 20?mm between areas by September. We examined the otoliths of the larval and age-0 stages of walleye pollock from these two areas in 2000 and 2001 to determine whether growth rate, hatch date, and/or temperature influenced fish size. Circulation models were used to determine whether transport of larvae from an upstream spawning group into the study areas could have occurred. Mean in situ temperature during sampling periods was not defined as a significant factor in altering growth rates. Overlapping hatch date distributions of the larval and age-0 fish in the Shumagin Island area confirmed that the fish were from the Shelikof Strait spawning group. Comparison of hatch date distributions in the upstream Sutwik Island area revealed larger/older larvae from an upstream spawning group mixed with larvae from the Shelikof Strait spawning group. Our results suggest that the offset of 20?mm SL between the groups of age-0 pollock was the result of a combination of enhanced survivorship of early-hatched larvae in the Sutwik area and the introduction and retention of the progeny of another spawning group originating upstream of Shelikof Strait.     

Infant parking and nesting, not allomaternal care, influence Malagasy primate life histories

Allomaternal care is a rare, though phylogenetically widespread, mammalian infant care strategy. Among primates, the effects of allomaternal care are marked; its presence correlates with faster infant growth, younger age at weaning, and shorter interbirth intervals. Recent comparative research has found that such fertility benefits are absent in other mammals and are thus unique to primates. In large part because data describing lemur allomaternal care were lacking, the reproductive advantages of allomaternal care have never been demonstrated in Malagasy strepsirrhines. Using newly available data and rigorous phylogenetic methods, we extend this hypothesis to strepsirrhines and test whether allomaternal care in lemurs confers similar maternal reproductive benefits. Contrary to expectations, the presence of allomaternal care did not significantly impact lemur reproductive output; we did not find relationships between allomaternal care and either fetal or postnatal growth rates or interbirth intervals. Rather, infant parking and nesting, strategies employed primarily by litter-bearing species, were positively associated with faster fetal and postnatal infant growth, while nesting was negatively associated with interbirth interval. Thus, although each form of haplorrhine allomaternal care is also observed in Malagasy primates, the effects that these behaviors have on female reproductive output more closely resemble nonprimate mammals. We suggest that Malagasy strepsirrhines may not equally benefit from allomaternal care compared to haplorrhines because reproductive rates are less flexible and allomaternal care may instead increase infant survival in Madagascar’s harsh and unpredictable environment. Our study has significant implications for understanding the evolution of infant care and developmental trajectories in mammals.     

Experimental evidence that workers recognize reproductives through cuticular hydrocarbons in the ant Odontomachus brunneus

Eusociality is characterized by a reproductive division of labor, wherein workers respond to the presence of reproductive individuals by refraining from reproduction themselves and restricting the reproductive efforts of others. Our understanding of how eusociality is maintained therefore depends on characterizing the mechanism by which workers detect the presence of a reproductive. Variations in cuticular hydrocarbons correspond to changes in reproductive ability in ants, and experimental studies are beginning to reveal the function of hydrocarbons as signals. In this study, we compare the cuticular hydrocarbon profiles of dominant and reproductive workers and queens of the ant Odontomachus brunneus with profiles of non-reproductive workers. Using split/reunification tests we document the existence of worker policing in both queenless and queenright colonies; supernumerary reproductives were treated aggressively by nestmates. Finally, we induce aggression and replicate queen-like submissive nestmate responses by supplementing the hydrocarbon profile of workers with (Z)-9-nonacosene, a compound that was significantly more abundant on the cuticles of reproductives. In three bioassays, we compare this manipulation to various control manipulations of the hydrocarbon profile and demonstrate that workers gauge the reproductive activity of nestmates through changes in their cuticular hydrocarbon profiles.     

Adoption and cuckoldry lead to alloparental care in the tessellated darter (Etheostoma olmstedi), a non-group-living species with no evidence of nest site limitation

While extensive empirical and theoretical work has focused on the evolution of costly cooperation (particularly in group-living species), less attention has been paid to more low-risk or immediately beneficial forms of cooperation. In some non-group-living darters, alloparental care (or allocare) by subordinates has been noted to result from by-product benefits as small territorial (subordinate) males adopt and provide care to the abandoned eggs of large territorial (dominant) males. In the tessellated darter (Etheostoma olmstedi), allocare also results from sneak fertilization. However, information on the rate of allocare by tessellated darters is contradictory: prior behavioral work suggested that it is very common, while a genetic examination showed males to primarily care for their own young. We found behavioral and genetic evidence of very high levels of allocare at our study location. The relative size of the assigned fathers of young to the alloparental male is consistent with the idea that initial allocare primarily results from sneak fertilization (“cuckoldry-based allocare”), but later allocare results from subordinate males caring at previously abandoned nests (“adoption-based allocare”). Larger males appeared to breed more frequently at different nests, but did not father more individual offspring than smaller males. Finally, low relatedness between abandoning and alloparenting males suggests that kin selection does not contribute to alloparental care. We discuss how variation in nest availability may explain the inconsistent findings of the rate of alloparental care in the tessellated darter, and how increased research in this and similar systems can expand our understanding of the evolution of cooperation.     

Evolution, radiation and chemotaxonomy of Lamellodysidea, a demosponge genus with anti-plasmodial metabolites

Sponges of the family Dysideidae (Dictyoceratida) are renowned for their diversity of secondary metabolites, and its genus Lamellodysidea, particularly Lamellodysidea herbacea, is the most studied taxon biochemically. Despite its importance, the taxonomic status of L. herbacea—whether it is a distinct species or a species complex—has never been assessed. Recent biochemical profiling revealed anti-plasmodial activity of brominated compounds in Lamellodysidea of the Pacific. Here, we present a comparative chemotaxonomic and molecular analysis of selected Dysideidae from the Pacific and the Indian Ocean (New Caledonia, Great Barrier Reef, Fiji, Mayotte, Guam, Palau). We investigated the phylogenetic relationships between the populations and assessed their bioactive (PBDE) compounds in order to unravel the taxonomic status of this commercially important group of sponges and assessed patterns of dispersal and biochemical variation. The molecular phylogeny was based on the internal transcribed ribosomal spacer and compared against a PBDE phylogeny for several specimens. Molecular data revealed a diversity of Indo-Pacific L. herbacea populations, also reflected by different PBDE compound profiles. Molecular and biochemical data also revealed a Lamellodysidea species new to science. Several specimens misidentified as Lamellodysidea were detected based on their position on different clades in the molecular phylogeny and their production of different halogenated compounds (brominated vs. chlorinated). The direct comparison of molecular and biochemical data also provided evidence for the occurrence of a host switch event and support for the theory that abiotic factors, such as sedimentation, affect the chemical constituents produced in L. herbacea.     

Understanding conservationists’ perspectives on the new‐conservation debate

A vibrant debate about the future direction of biodiversity conservation centers on the merits of the so‐called new conservation. Proponents of the new conservation advocate a series of positions on key conservation ideas, such as the importance of human‐dominated landscapes and conservation's engagement with capitalism. These have been fiercely contested in a debate dominated by a few high‐profile individuals, and so far there has been no empirical exploration of existing perspectives on these issues among a wider community of conservationists. We used Q methodology to examine empirically perspectives on the new conservation held by attendees at the 2015 International Congress for Conservation Biology (ICCB). Although we identified a consensus on several key issues, 3 distinct positions emerged: in favor of conservation to benefit people but opposed to links with capitalism and corporations, in favor of biocentric approaches but with less emphasis on wilderness protection than prominent opponents of new conservation, and in favor of the published new conservation perspective but with less emphasis on increasing human well‐being as a goal of conservation. Our results revealed differences between the debate on the new conservation in the literature and views held within a wider, but still limited, conservation community and demonstrated the existence of at least one viewpoint (in favor of conservation to benefit people but opposed to links with capitalism and corporations) that is almost absent from the published debate. We hope the fuller understanding we present of the variety of views that exist but have not yet been heard, will improve the quality and tone of debates on the subject.     

Reservoir‐host amplification of disease impact in an endangered amphibian

Emerging wildlife pathogens are an increasing threat to biodiversity. One of the most serious wildlife diseases is chytridiomycosis, caused by the fungal pathogen, Batrachochytrium dendrobatidis (Bd), which has been documented in over 500 amphibian species. Amphibians vary greatly in their susceptibility to Bd; some species tolerate infection, whereas others experience rapid mortality. Reservoir hosts—species that carry infection while maintaining high abundance but are rarely killed by disease—can increase extinction risk in highly susceptible, sympatric species. However, whether reservoir hosts amplify Bd in declining amphibian species has not been examined. We investigated the role of reservoir hosts in the decline of the threatened northern corroboree frog (Pseudophryne pengilleyi) in an amphibian community in southeastern Australia. In the laboratory, we characterized the response of a potential reservoir host, the (nondeclining) common eastern froglet (Crinia signifera), to Bd infection. In the field, we conducted frog abundance surveys and Bd sampling for both P. pengilleyi and C. signifera. We built multinomial logistic regression models to test whether Crinia signifera and environmental factors were associated with P. pengilleyi decline. C. signifera was a reservoir host for Bd. In the laboratory, many individuals maintained intense infections (>1000 zoospore equivalents) over 12 weeks without mortality, and 79% of individuals sampled in the wild also carried infections. The presence of C. signifera at a site was strongly associated with increased Bd prevalence in sympatric P. pengilleyi. Consistent with disease amplification by a reservoir host, P. pengilleyi declined at sites with high C. signifera abundance. Our results suggest that when reservoir hosts are present, population declines of susceptible species may continue long after the initial emergence of Bd, highlighting an urgent need to assess extinction risk in remnant populations of other declined amphibian species.     

Trait space of rare plants in a fire‐dependent ecosystem

The causes of species rarity are of critical concern because of the high extinction risk associated with rarity. Studies examining individual rare species have limited generality, whereas trait‐based approaches offer a means to identify functional causes of rarity that can be applied to communities with disparate species pools. Differences in functional traits between rare and common species may be indicative of the functional causes of species rarity and may therefore be useful in crafting species conservation strategies. However, there is a conspicuous lack of studies comparing the functional traits of rare species and co‐occurring common species. We measured 18 important functional traits for 19 rare and 134 common understory plant species from North Carolina's Sandhills region and compared their trait distributions to determine whether there are significant functional differences that may explain species rarity. Flowering, fire, and tissue‐chemistry traits differed significantly between rare and common, co‐occurring species. Differences in specific traits suggest that fire suppression has driven rarity in this system and that changes to the timing and severity of prescribed fire may improve conservation success. Our method provides a useful tool to prioritize conservation efforts in other systems based on the likelihood that rare species are functionally capable of persisting.