Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog

The recently-emerged amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has had an unprecedented impact on global amphibian populations, and highlights the urgent need to develop effective mitigation strategies. We conducted in-situ antifungal treatment experiments in wild populations of the endangered mountain yellow-legged frog during or immediately after Bd-caused mass die-off events. The objective of treatments was to reduce Bd infection intensity (“load”) and in doing so alter frog-Bd dynamics and increase the probability of frog population persistence despite ongoing Bd infection. Experiments included treatment of early life stages (tadpoles and subadults) with the antifungal drug itraconazole, treatment of adults with itraconazole, and augmentation of the skin microbiome of subadults with Janthinobacterium lividum, a commensal bacterium with antifungal properties. All itraconazole treatments caused immediate reductions in Bd load, and produced longer-term effects that differed between life stages. In experiments focused on early life stages, Bd load was reduced in the 2 months immediately following treatment and was associated with increased survival of subadults. However, Bd load and frog survival returned to pre-treatment levels in less than 1 year, and treatment had no effect on population persistence. In adults, treatment reduced Bd load and increased frog survival over the entire 3-year post-treatment period, consistent with frogs having developed an effective adaptive immune response against Bd. Despite this protracted period of reduced impacts of Bd on adults, recruitment into the adult population was limited and the population eventually declined to near-extirpation. In the microbiome augmentation experiment, exposure of subadults to a solution of J. lividum increased concentrations of this potentially protective bacterium on frogs. However, concentrations declined to baseline levels within 1 month and did not have a protective effect against Bd infection. Collectively, these results indicate that our mitigation efforts were ineffective in causing long-term changes in frog-Bd dynamics and increasing population persistence, due largely to the inability of early life stages to mount an effective immune response against Bd. This results in repeated recruitment failure and a low probability of population persistence in the face of ongoing Bd infection.

Trailing-edge zombie forests can increase population persistence in the face of climate change

Climate-driven habitat shifts pose challenges for dispersal-limited, late-maturing taxa such as trees. Older trees are often the most reproductive individuals in the population, but as habitats shift, these individuals can be left behind in the trailing range edge, generating "zombie forests" that may persist long after the suitable habitat has shifted. Are these zombie forests vestiges of ecosystems past or do they play an ecological role? To understand how zombie forests affect population persistence, we developed a spatially explicit, stage-structured model of tree populations occupying a shifting habitat. Our model shows that seed dispersal from zombie forests to the range core can considerably increase the maximum rate of climate change that a population can withstand. Moreover, the entire core population can ultimately descend from recruitment-limited zombie forests, highlighting their demographic value. Our results suggest that preserving trailing-edge zombie forests can greatly increase population persistence in the face of climate change.

Modeling Oyster Reef Restoration: Larval Supply and Reef Geometry Jointly Determine Population Resilience and Performance

Restoration of native oyster (Crassostrea virginica) populations in Chesapeake Bay shows great promise after three decades of failed attempts. Population models used to inform oyster restoration had integrated reef habitat quality, demonstrating that reef height determines oyster population persistence and resilience. Larval recruitment drives population dynamics of marine species, yet its impact with reef height and sediment deposition upon reef restoration is unknown. To assess the influence of reef height, sediment deposition and larval supply, we adapted a single-stage population model to incorporate stage structure using a system of four differential equations modeling change in juvenile density (J), and changes in volume of adults (A), oyster shell reef (R), and sediment (S) on an oyster reef. The JARS model was parameterized with empirical data from field experiments. Larval supply included larvae from the natal population and from outside populations. The stage-structured model possessed multiple non-negative equilibria (i.e., alternative stable states). Different initial conditions (e.g., oyster shell reef height) resulted in different final states. The main novel findings were that the critical reef height for population persistence and resilience was jointly dependent on sediment input and larval supply. A critical minimum larval supply was necessary for a reef to persist, even when initial sediment deposition was zero. As larval supply increased, the initial reef height needed for reef persistence was lowered, and oyster reef resilience was enhanced. A restoration oyster reef with higher larval influx could recover from more severe disturbances than a reef with lower larval influx. To prevent local extinction and assure a positive population state, higher levels of larval supply were required at greater sediment concentrations to overcome the negative effects of sediment accumulation on the reef. In addition, reef persistence was negatively related to sediment deposited on a reef prior to larval settlement and recruitment, implying that restoration reefs should be constructed immediately before settlement and recruitment to minimize sediment accumulation on a reef before settlement. These findings are valuable in oyster reef restoration because they can guide reef construction relative to larval supply and sediment deposition on a reef to yield effective and cost-efficient restoration strategies.

Female fruit flies cannot protect stored sperm from high temperature damage

Recently, it has been demonstrated that heat-induced male sterility is likely to shape population persistence as climate change progresses. However, an under-explored possibility is that females may be able to successfully store and preserve sperm at temperatures that sterilise males, which could ameliorate the impact of male infertility on populations. Here, we test whether females from two fruit fly species can protect stored sperm from a high temperature stress. We find that sperm carried by female Drosophila virilis are almost completely sterilised by high temperatures, whereas sperm carried by female Zaprionus indianus show only slightly reduced fertility. Heat-shocked D. virilis females can recover fertility when allowed to remate, suggesting that the delivered heat-shock is destroying stored sperm and not directly damaging females in this species. The temperatures required to reduce fertility of mated females are substantially lower than the temperatures required to destroy mature sperm in males, suggesting that females are worse than males at protecting mature sperm. This suggests that female sperm storage is unlikely to ameliorate the impacts of high temperature fertility losses in males, and instead exacerbates fertility costs of high temperatures, representing an important determinant of population persistence during climate change.

Effectiveness of antifungal treatments during chytridiomycosis epizootics in populations of an endangered frog

The recently-emerged amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has had an unprecedented impact on global amphibian populations, and highlights the urgent need to develop effective mitigation strategies against this pathogen. We conducted field antifungal treatment experiments in populations of the endangered mountain yellow-legged frog during or immediately after Bd-caused mass die-off events. The objective of the treatments was to reduce Bd infection intensity ("load") and in doing so alter frog-Bd dynamics and increase the probability of frog population persistence despite ongoing Bd infection. Experiments included treatment of early life stages (tadpoles and subadults) with the antifungal drug itraconazole, treatment of adults with itraconazole, and augmentation of the skin microbiome of subadults with Janthinobacterium lividum, a commensal bacterium with antifungal properties. All itraconazole treatments caused immediate reductions in Bd load, and produced longer-term effects that differed between life stages. In experiments focused on early life stages, Bd load was reduced in the two months immediately following treatment and was associated with increased survival of subadults. However, Bd load and frog survival returned to pre-treatment levels in less than one year, and treatment had no effect on population persistence. In adults, treatment reduced Bd load and increased frog survival over the three-year post-treatment period, consistent with frogs having developed an effective adaptive immune response against Bd. Despite this protracted period of reduced impacts of Bd on adults, recruitment of new individuals into the adult population was limited and the population eventually declined to near-extirpation. In the microbiome augmentation experiment, bathing frogs in a J. lividum solution after Bd load reduction with itraconazole increased concentrations of this bacterium on frogs, but concentrations declined to baseline levels within one month and did not have a protective effect against Bd infection. Collectively, these results suggest that Bd mitigation efforts focused on frog populations that have recently declined due to Bd emergence are ineffective in causing long-term changes in frog-Bd dynamics and increasing population persistence, due largely to the inability of early life stages to mount an effective immune response against Bd and resulting high susceptibility. This results in repeated recruitment failure and a low probability of population persistence in the face of ongoing Bd infection.

Forest management affects seasonal source-sink dynamics in a territorial, group-living bird

The persistence of wildlife populations is under threat as a consequence of human activities, which are degrading natural ecosystems. Commercial forestry is the greatest threat to biodiversity in boreal forests. Forestry practices have degraded most available habitat, threatening the persistence of natural populations. Understanding population responses is, therefore, critical for their conservation. Population viability analyses are effective tools to predict population persistence under forestry management. However, quantifying the mechanisms driving population responses is complex as population dynamics vary temporally and spatially. Metapopulation dynamics are governed by local dynamics and spatial factors, potentially mediating the impacts of forestry e.g., through dispersal. Here, we performed a seasonal, spatially explicit population viability analysis, using long-term data from a group-living territorial bird (Siberian jay, Perisoreus infaustus). We quantified the effects of forest management on metapopulation dynamics, via forest type-specific demography and spatially explicit dispersal, and how forestry impacted the stability of metapopulation dynamics. Forestry reduced metapopulation growth and stability, through negative effects on reproduction and survival. Territories in higher quality natural forest contributed more to metapopulation dynamics than managed forests, largely through demographic processes rather than dispersal. Metapopulation dynamics in managed forest were also less resilient to disturbances and consequently, may be more vulnerable to environmental change. Seasonal differences in source-sink dynamics observed in managed forest, but not natural forests, were caused by associated seasonal differences in dispersal. As shown here, capturing seasonal source-sink dynamics allows us to predict population persistence under human disturbance and to provide targeted conservation recommendations.