Recent publications in Zoology and Ecology

Laurance, William F., and Van Oosterzee, Penny (2019) How Indonesia’s election puts global biodiversity at stake with an impending war on palm oil. The Conversation.
Almost overnight, Jokowi has transformed from an environmental good-guy — someone who’s battled destructive wildfires and noxious haze, tried to slow palm oil expansion and promoted several other eco-smart measures — into a nationalistic mouthpiece for the oil palm industry. Let’s hope this ‘Dr Jekyll and Mr Hyde’ transformation of Jokowi is temporary — a kind of fleeting election madness that overtakes many politicians in the heat of battle. If not, Indonesia’s forests and the endangered species living in them will be at even more risk.

Sloan, Sean, Campbell, Mason, Alamgir, Mohammed, Egerton, Jayden, Ishida, Yoko, Senn, Nicole, Huther, Jaime, and Laurance, William F. (2019) Hidden challenges for conservation and development along the Trans-Papuan economic corridor. Environmental Science & Policy, 92. pp. 98-106.
The island of New Guinea harbours one of the world’s largest tracts of intact tropical forest, with 41% of its land area in Indonesian Papua (Papua and Papua Barat Provinces). Within Papua, the advent of a 4000-km ‘development corridor’ reflects a national agenda promoting primary-resource extraction and economic integration. Papua, a resource frontier containing vast forest and mineral resources, increasingly exhibits new conservation and development dynamics suggestive of the earlier frontier development phases of other Indonesian regions. Local environmental and social considerations have been discounted in the headlong rush to establish the corridor and secure access to natural resources. Peatland and forest conversion are increasingly extensive within the epicentres of economic development. Deforestation frontiers are emerging along parts of the expanding development corridor, including within the Lorentz World Heritage Site. Customary land rights for Papua’s indigenous people remain an afterthought to resource development, fomenting conditions contrary to conservation and sustainable development. A centralised development agenda within Indonesia underlies virtually all of these changes. We recommend specific actions to address the environmental, economic, and socio-political challenges of frontier development along the Papuan corridor.

Pirrota, Vanessa, Grech, Alana, Jonsen, Ian D., Laurance, William F., and Harcourt, Robert G. (2019) Consequences of global shipping traffic for marine giants. Frontiers in Ecology and the Environment, 17 (1). pp. 39-47.
Shipping routes in the ocean are analogous to terrestrial roads, in that they are regularly used thoroughfares that concentrate the movement of vessels between multiple locations. We applied a terrestrial road ecology framework to examine the ecological impacts of increased global shipping on "marine giants" (ie great whales, basking sharks [Cetorhinus maximus], and whale sharks [Rhincodon typus]). This framework aided in identifying where such "marine roads" and marine giants are likely to interact and the consequences of those interactions. We also reviewed known impacts of shipping routes on these species, and then applied the road ecology framework to detect unknown and potentially threatening processes. In the marine environment, such a framework can be used to incorporate knowledge of existing shipping impacts into management practices, thereby reducing the detrimental effects of future expansion of shipping routes on marine giants.

Congdon, B.C. (2019) Seabirds. In: Hutchings, Pat, Kingsford, Michael, and Hoegh-Guldberg, Ove, (eds.) The Great Barrier Reef: biology, environment and management. CSIRO, Melbourne, VIC, Australia, pp. 419-429.
[Extract]Seabirds are highly visible, charismatic predators in marine ecosystems that feed primarily or exclusively at sea. They have a range of relatively unique life-history characteristics associated with this marine lifestyle. Many of these characteristics are directly linked with having to forage over large distances to obtain sufficient food to breed.

Ni, Yijun, Ma, Xiaolin, Hu, Wei, Blair, David, and Yin, Mingbo (2019) New lineages and old species: lineage diversity and regional distribution of Moina (Crustacea: Cladocera) in China. Molecular Phylogenetics and Evolution, 134. pp. 87-98.
The distribution and genetic diversity of freshwater zooplankton is understudied in the Eastern Palearctic. Here, we explored the lineage diversity and regional distribution of the genus Moina in China. Members of this genus are often keystone components of freshwater ecosystems and have been frequently subjected to toxicological and physiological studies. Four species of Moina were identified, based on morphology, in 50 of 113 Chinese water bodies examined, and their phylogenetic position was analyzed using both a mitochondrial (mitochondrial cytochrome c oxidase subunit I; COI) and a nuclear marker (the nuclear internal transcribed spacer; ITS-1). Both molecular markers identified four clades corresponding broadly to the morphological species. Mitochondrial DNA analysis showed the presence of four species complexes with eleven lineages across China, five of which were new. However, some lineages (and even individual haplotypes) were widespread in Eurasia, suggesting an ability to disperse over long distances. In contrast, a few lineages exhibited restricted distributions. The nuclear phylogeny also recognized four species of Moina within China and seven very distinct clades. Interestingly, one specimen possessing Moina cf. micrura mtDNA had ITS-1 alleles of the M. cf. brachiata clade. This discordance between mtDNA and nuclear ITS-1 phylogenies is indicative of interspecific introgression and hybridization. Additionally, our COI phylogeny showed apparent paraphyly in two Moina species groups, suggesting introgression of their mitochondrial genomes. Our data shows the regional distribution/diversity of the Moina species complex in a Eurasian context.

Alamgir, Mohammed, Campbell, Mason J., Sloan, Sean, Suhardiman, Ali, Supriatna, Jatna, and Laurance, William F. (2019) High-risk infrastructure projects pose imminent threats to forests in Indonesian Borneo. Scientific Reports, 9. 140. pp. 1-10.
Indonesian Borneo (Kalimantan) sustains ~37 million hectares of native tropical forest. Numerous large-scale infrastructure projects aimed at promoting land-development activities are planned or ongoing in the region. However, little is known of the potential impacts of this new infrastructure on Bornean forests or biodiversity. We found that planned and ongoing road and rail-line developments will have many detrimental ecological impacts, including fragmenting large expanses of intact forest. Assuming conservatively that new road and rail projects will influence only a 1 km buffer on either side, landscape connectivity across the region will decline sharply (from 89% to 55%) if all imminently planned projects proceed. This will have particularly large impacts on wide-ranging, rare species such as rhinoceros, orangutans, and elephants. Planned developments will impact 42 protected areas, undermining Indonesian efforts to achieve key targets under the Convention on Biological Diversity. New infrastructure will accelerate expansion in intact or frontier regions of legal and illegal logging and land colonization as well as illicit mining and wildlife poaching. The net environmental, social, financial, and economic risks of several imminent projects—such as parallel border roads in West, East, and North Kalimantan, new Trans-Kalimantan road developments in Central Kalimantan and North Kalimantan, and freeways and rail lines in East Kalimantan—could markedly outstrip their overall benefits. Such projects should be reconsidered in light of rigorous cost-benefit frameworks.

Maxwell, Stephen J., Dekkers, Aart M., Rymer, Tasmin L., and Congdon, Bradley C. (2019) Laevistrombus Abbott 1960 (Gastropoda: Strombidae): Indian and southwest Pacific species. Zootaxa, 4555 (4). pp. 491-506.
Here we evaluate the taxonomy of the marine gastropod genus Laevistrombus Abbott, 1960 and determine that there are five extant species within this genus, three of which occur in the southwest Pacific. Comparative analyses of this complex have been problematic due to the lack of designated type material. Therefore, we present the type material for L. canarium Linnaeus, 1758; L. taeniatus Quoy & Gaimard, 1834; and L. vanikorensis Quoy & Gaimard, 1834. Current taxonomy has L. vanikorensis absorbed within the L. canarium complex. L. taeniatus is generally held to be a synonym of L. turturella Röding, 1789. We demonstrate that both L. taeniatus and L. vanikorensis are distinct species and reinstate both to species level. Our revision also notes the significant variability in early teleoconch structure within the geographic range of L. vanikorensis, and highlights the need for a greater revision of Laevistrombus, given the diversity in early teleoconch morphology present in southwest Pacific species.

Liu, JiaJia, Lindenmayer, David B., Yang, Wenjing, Ren, Yuan, Campbell, Mason J., Wu, Chuping, Luo, Yangqing, Zhong, Lei, and Yu, Mingjian (2019) Diversity and density patterns of large old trees in China. Science of the Total Environment, 655. pp. 255-262.
Large old trees are keystone ecological structures that provide vital ecosystem services to humans. However, there are few large-scale empirical studies on patterns of diversity and density of large old trees in human-dominated landscapes. We present the results of the first nationwide study in China to investigate the patterns of diversity and density of large old trees in human-dominated landscapes. We collated data on 682,730 large trees ≥100 years old from 198 Chinese regions to quantify tree species diversity, tree density and maximum tree age patterns. We modelled the effects of natural environmental variables (e.g. climate and topography) and anthropogenic variables (e.g. human population density and city age) on these measures. We found a low density of large old trees across study regions (0.36 trees/km2), and large variation in species richness among regions (ranging from 1 to 232 species). More than 95% of trees were <500 years old. The best fit models showed that: (1) Species diversity (species richness adjusted by region size) was positively associated with mean annual rainfall and city age; (2) Density of clustered trees, which are mostly remnants of ancient woods, was negatively influenced by human population density and rural population (% of total population). In contrast, the density of scattered trees, which are mostly managed by local people, was positively correlated with mean annual rainfall and human population density. To better protect large old trees in cities and other highly-populated areas, conservation policy should protect ancient wood remnants, mitigate the effects environmental change (e.g. habitat fragmentation), minimize the negative effects of human activities (e.g. logging), and mobilize citizens to participate in conservation activities (e.g. watering trees during droughts).

Laurance, William F. (2019) Climate change is killing off Earth’s little creatures. The Conversation.
But a global review of insect research has found another casualty: 40% of insect species are declining and a third are endangered. It confirms what many have been suspecting: in Australia and around the world, arthropods – which include insects, spiders,centipedes and the like — appear to be in trouble.

Cornelis, Jari, Nordberg, Eric J., and Schwarzkopf, Lin (2019) Antipredator behaviour of invasive geckos in response to chemical cues from snakes. Ethology, 125 (1). pp. 57-63.
Antipredator behaviours and the ability to appropriately assess predation risk contribute to increased fitness. Predator avoidance can be costly; however, so we expect prey to most strongly avoid predators that pose the greatest risk (i.e., prey should show threat sensitivity). For invasive species, effectively assessing the relative risk posed by predators in the new environment may help them establish in new environments. We examined the antipredator behaviour of introduced Asian house geckos, Hemidactylus frenatus (Schlegel), by determining if they avoided shelters scented with the chemical cues of native predatory snakes (spotted pythons, Antaresia maculosa [Peters]; brown tree snakes, Boiga irregularis [Merrem]; common tree snakes, Dendrelaphis punctulata [Grey]; and carpet pythons, Morelia spilota [Lacepede]). We also tested if Asian house geckos collected from vegetation vs. anthropogenic substrates (buildings) responded differently to the chemical cues of predatory snakes. Asian house geckos did not show a generalised antipredator response, that is, they did not respond to the chemical cues of all snakes in the same way. Asian house geckos avoided the chemical cues of carpet pythons more strongly than those of other snake species, providing some support for the threat-sensitivity hypothesis. There was no difference in the antipredator behaviour of Asian house geckos collected from buildings vs. natural vegetation, suggesting that individuals that have invaded natural habitats have not changed their antipredator behaviour compared to urban individuals. Overall, we found some evidence indicating Asian house geckos are threat-sensitive to some Australian predacious snakes.

Laurance, William F. (2019) A highway megaproject tears at the heart of New Guinea’s rainforest. Yale Environment 360.
The Indonesian government is building a 2,700-mile road network on the island of New Guinea, opening up some of the world’s last great tropical rainforests to development and threatening unique indigenous cultures. Can international pressure force Indonesia to scale back this megaproject?

Laurance, Bill, and Salt, David (2019) Hacking the illegal trade in wildlife. Australasian Science, 40. pp. 32-33.
[Extract] Hackers should be deployed to disrupt a $23 billion online market in wildlife and wildlife part. All around the world, forests and other ecosystems are falling silent, their wildlife populations decimated by illegal hunting and wildlife trading.

Mukul, Sharif A., Alamgir, Mohammed, Sohel, Md. Shawkat I., Pert, Petina L., Herbohn, John, Turton, Stephen M., Khan, Md. Saiful I., Munim, Shifath Ahmed, Reza, A.H.M. Ali, and Laurance, William F. (2019) Combined effects of climate change and sea-level rise project dramatic habitat loss of the globally endangered Bengal tiger in the Bangladesh Sundarbans. Science of the Total Environment, 663. pp. 830-840.
The Sundarbans, in southern coastal Bangladesh, is the world's largest surviving mangrove habitat and the last stronghold of tiger adapted to living in a mangrove ecosystem. Using MaxEnt (maximum entropy modeling), current distribution data, land-use/land cover and bioclimatic variables, we modeled the likely future distribution of the globally endangered Bengal tiger (Panthera tigris tigris) in the Bangladesh Sundarbans. We used two climatic scenarios (i.e., RCP6.0 and RCP8.5) developed by the Intergovernmental Panel on Climate Change (IPCC) to provide projections of suitable habitats of Bengal tigers in 2050 and 2070. We also combined projected sea-level rise for the area in our models of future species distributions. Our results suggest that there will be a dramatic decline in suitable Bengal tiger habitats in the Bangladesh Sundarbans. Other than various aspects of local climate, sea-level rise is projected to have a substantial negative impact on Bengal tiger habitats in this low-lying area. Our model predicts that due to the combined effect of climate change and sea-level rise, there will be no suitable Bengal tiger habitat remaining in the Sundarbans by 2070. Enhancing terrestrial protected area coverage, regular monitoring, law enforcement, awareness-building among local residents among the key strategies needed to ensure long-term survival and conservation of the Bengal tiger in the Bangladesh Sundarbans.

Nigenda-Morales, Sergio F., Gompper, Matthew E., Valenzuela-Galván, David, Lay, Anna R., Kapheim, Karen M., Hass, Christine, Booth-Binczik, Susan D., Binczik, Gerald A., Hirsch, Ben T., McColgin, Maureen, Koprowski, John L., McFadden, Katherine, Wayne, Robert K., and Koepfli, Klaus-Peter (2019) Phylogeographic and diversification patterns of the white-nosed coati (Nasua narica): evidence for south-to-north colonization of North America. Molecular Phylogenetics and Evolution, 131. pp. 149-163.
White-nosed coatis (Nasua narica) are widely distributed throughout North, Central, and South America, but the patterns of temporal and spatial diversification that have contributed to this distribution are unknown. In addition, the biogeographic history of procyonid species in the Americas remains contentious. Using sequences from three mitochondrial loci (Cytochrome b, NAHD5 and 16S rRNA; 2201 bp) and genotypes from 11 microsatellite loci, we analyzed genetic diversity to determine phylogeographic patterns, genetic structure, divergence times, and gene flow among Nasua narica populations throughout the majority of the species' range. We also estimated the ancestral geographic range of N. narica and other procyonid species. We found a high degree of genetic structure and divergence among populations that conform to five evolutionarily significant units. The most southerly distributed population (Panama) branched off much earlier (similar to 3.8 million years ago) than the northern populations (< 1.2 million years ago). Estimated gene flow among populations was low and mostly northwards and westwards. The phylogeographic patterns within N. narica are associated with geographic barriers and habitat shifts likely caused by Pliocene-Pleistocene climate oscillations. Significantly, our findings suggest the dispersal of N. narica was south-to-north beginning in the Pliocene, not in the opposite direction during the Pleistocene as suggested by the fossil record, and that the most recent common ancestor for coati species was most likely distributed in South or Central America six million years ago. Our study implies the possibility that the diversification of Nasua species, and other extant procyonid lineages, may have occurred in South America.

Smith, Nicholas G., Keenan, Trevor F., Prentice, I. Colin, Wang, Han, Wright, Ian J., Niinemets, Ülo, Crous, Kristine Y., Domingues, Tomas F., Guerrieri, Rossella, Ishida, F. Yoko, Kattge, Jens, Kruger, Eric L., Maire, Vincent, Rogers, Alistair, Serbin, Shawn P., Tarvainen, Lasse, Togashi, Henrique F., Townsend, Philip A., Wang, Meng, Weerasinghe, Lasantha K., and Zhou, Shuang-Xi (2019) Global photosynthetic capacity is optimized to the environment. Ecology Letters, 22 (3). pp. 506-517.
Earth system models (ESMs) use photosynthetic capacity, indexed by the maximum Rubisco carboxylation rate (Vcmax), to simulate carbon assimilation and typically rely on empirical estimates, including an assumed dependence on leaf nitrogen determined from soil fertility. In contrast, new theory, based on biochemical coordination and co‐optimization of carboxylation and water costs for photosynthesis, suggests that optimal Vcmax can be predicted from climate alone, irrespective of soil fertility. Here, we develop this theory and find it captures 64% of observed variability in a global, field‐measured Vcmax dataset for C3 plants. Soil fertility indices explained substantially less variation (32%). These results indicate that environmentally regulated biophysical constraints and light availability are the first‐order drivers of global photosynthetic capacity. Through acclimation and adaptation, plants efficiently utilize resources at the leaf level, thus maximizing potential resource use for growth and reproduction. Our theory offers a robust strategy for dynamically predicting photosynthetic capacity in ESMs.

Nordberg, Eric J., and Schwarzkopf, Lin (2019) Reduced competition may allow generalist species to benefit from habitat homogenization. Journal of Applied Ecology, 56 (2). pp. 305-318.
Complex environments support high biodiversity and diverse microhabitat availability, which may reduce the intensity of competition among species. Both natural and anthropogenic disturbances reduce the structural complexity of habitats, leading to homogenization. High abundances of common, generalist species in disturbed habitats may be driven by reduced competition from specialists in similar habitats. We quantified habitat availability for and utilization of three co‐occurring arboreal geckos (Australian native house geckos [Gehyra dubia], northern velvet geckos [Oedura castelnaui] and eastern spiny‐tailed geckos [Strophurus williamsi]) in four replicated grazing regimes in an experimental grazing trial in north‐east Queensland, Australia. Native house geckos were most abundant in heavily grazed habitats, whereas the two other species rarely co‐occurred (either with each other or with native house geckos). Geckos displayed resource partitioning of habitat features, such as tree species and structural characteristics. We found evidence of interspecific competition among gecko species, in which native house geckos shifted their habitat selection in the presence of velvet geckos. In the absence of other geckos, native house geckos preferred rough, peeling bark and dead trees, yet in the presence of velvet geckos, native house geckos shifted away from dead trees, and used more structurally complex trees, probably due to high niche overlap with velvet geckos. Native house geckos were more resistant to the negative effects of livestock grazing than either velvet or spiny‐tailed geckos. In the absence of other species, native house geckos used a wider range of microhabitats. Synthesis and applications. Species assemblages are often the results of multiple or complex factors, including predation pressure, habitat availability or competitive interactions. The homogenizing effects on habitat structure caused by livestock grazing reduce diversity and suitability for microhabitat specialists. Reduced competition can therefore promote the abundance of microhabitat generalist species, such as Australian native house geckos, suggesting that livestock grazing leads to homogenization and simplification of habitat structure, which ultimately leads to changes in species composition through reduced competition. Understanding species’ responses to disturbance, and more broadly, habitat complexity, is crucial for maintaining or increasing biological diversity in anthropogenically modified landscapes.

Nuske, S.J., Anslan, S., Tedersoo, L., Congdon, B.C., and Abell, S.E. (2019) Ectomycorrhizal fungal communities are dominated by mammalian dispersed truffle-like taxa in north-east Australian woodlands. Mycorrhiza, 29. pp. 181-193.
Mycorrhizal fungi are very diverse, including those that produce truffle-like fruiting bodies. Truffle-like fungi are hypogeous and sequestrate (produced below-ground, with an enclosed hymenophore) and rely on animal consumption, mainly by mammals, for spore dispersal. This dependence links mycophagous mammals to mycorrhizal diversity and, assuming truffle-like fungi are important components of mycorrhizal communities, to plant nutrient cycling and ecosystem health. These links are largely untested as currently little is known about mycorrhizal fungal community structure and its dependence on mycophagous mammals. We quantified the mycorrhizal fungal community in the north-east Australian woodland, including the portion interacting with ten species of mycophagous mammals. The study area is core habitat of an endangered fungal specialist marsupial, Bettongia tropica, and as such provides baseline data on mycorrhizal fungi-mammal interactions in an area with no known mammal declines. We examined the mycorrhizal fungi in root and soil samples via high-throughput sequencing and compared the observed taxa to those dispersed by mycophagous mammals at the same locations. We found that the dominant root-associating ectomycorrhizal fungal taxa (> 90% sequence abundance) included the truffle-like taxa Mesophellia, Hysterangium and Chondrogaster. These same taxa were also present in mycophagous mammalian diets, with Mesophellia often dominating. Altogether, 88% of truffle-like taxa from root samples were shared with the fungal specialist diet and 52% with diets from generalist mammals. Our data suggest that changes in mammal communities, particularly the loss of fungal specialists, could, over time, induce reductions to truffle-like fungal diversity, causing ectomycorrhizal fungal communities to shift with unknown impacts on plant and ecosystem health.

Maron, Martine, Griffin, Andrea, Reside, April, Laurance, Bill, Driscoll, Don, Ritchie, Euan, and Turton, Steve (2019) To reduce fire risk and meet climate targets, over 300 scientists call for stronger land clearing laws. The Conversation.
Australia’s high rates of forest loss and weakening land clearing laws are increasing bushfire risk, and undermining our ability to meet national targets aimed at curbing climate change. This dire situation is why we are among the more than 300 scientists and practitioners who have signed a declaration calling for governments to restore, or better strengthen regulations to protect native vegetation.

Pardo Vargas, Lain Efrain, de Oliveira Roque, Fabio, Campbell, Mason, and Laurance, William F. (2019) Response to correspondence letter “species responses to oil palm: cautionary considerations for multi-site extrapolation”. Biological Conservation, 229. pp. 181-182.
We appreciate the correspondence related to our paper (Pardo et al., 2018a), which raises three main concerns about our work: 1) an apparent extrapolation of the information we gathered in the Llanos region of Colombia to the entire country; 2) a putative limitation in our study design; and 3) a criticism of what was characterized as a misleading focus on non-threatened species. Below we address each criticism in turn.

Bloomfield, Keith J., Prentice, I. Colin, Cernusak, Lucas A., Eamus, Derek, Medlyn, Belinda E., Rumman, Rizwana, Wright, Ian J., Boer, Matthias M., Cale, Peter, Cleverly, James, Egerton, John J.G., Ellsworth, David S., Evans, Bradley J., Hayes, Lucy S., Hutchinson, Michael F., Liddell, Michael J., Macfarlane, Craig, Meyer, Wayne S., Togashi, Henrique F., Wardlaw, Tim, Zhu, Lingling, and Atkin, Owen K. (2019) The validity of optimal leaf traits modelled on environmental conditions. New Phytologist, 221 (3). pp. 1409-1423.
The ratio of leaf intercellular to ambient CO2 (χ) is modulated by stomatal conductance (gs). These quantities link carbon (C) assimilation with transpiration, and along with photosynthetic capacities (Vcmax and Jmax) are required to model terrestrial C uptake. We use optimization criteria based on the growth environment to generate predicted values of photosynthetic and water‐use efficiency traits and test these against a unique dataset. Leaf gas‐exchange parameters and carbon isotope discrimination were analysed in relation to local climate across a continental network of study sites. Sun‐exposed leaves of 50 species at seven sites were measured in contrasting seasons. Values of χ predicted from growth temperature and vapour pressure deficit were closely correlated to ratios derived from C isotope (δ13C) measurements. Correlations were stronger in the growing season. Predicted values of photosynthetic traits, including carboxylation capacity (Vcmax), derived from δ13C, growth temperature and solar radiation, showed meaningful agreement with inferred values derived from gas‐exchange measurements. Between‐site differences in water‐use efficiency were, however, only weakly linked to the plant's growth environment and did not show seasonal variation. These results support the general hypothesis that many key parameters required by Earth system models are adaptive and predictable from plants' growth environments.

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