Interconnecting global threats: climate change, biodiversity loss, and infectious diseases.

The concurrent pressures of rising global temperatures, rates and incidence of species decline, and emergence of infectious diseases represent an unprecedented planetary crisis. Intergovernmental reports have drawn focus to the escalating climate and biodiversity crises and the connections between them, but interactions among all three pressures have been largely overlooked. Non-linearities and dampening and reinforcing interactions among pressures make considering interconnections essential to anticipating planetary challenges. In this Review, we define and exemplify the causal pathways that link the three global pressures of climate change, biodiversity loss, and infectious disease. A literature assessment and case studies show that the mechanisms between certain pairs of pressures are better understood than others and that the full triad of interactions is rarely considered. Although challenges to evaluating these interactions-including a mismatch in scales, data availability, and methods-are substantial, current approaches would benefit from expanding scientific cultures to embrace interdisciplinarity and from integrating animal, human, and environmental perspectives. Considering the full suite of connections would be transformative for planetary health by identifying potential for co-benefits and mutually beneficial scenarios, and highlighting where a narrow focus on solutions to one pressure might aggravate another.

Not just range limits: Warming rate and thermal sensitivity shape climate change vulnerability in a species range center.

Climate change manifests unevenly across space and time and produces complex patterns of stress for ecological systems. Species can also show substantial among-population variability in response to environmental change across their geographic range due to evolutionary processes. Explanatory factors or their proxies, such as temperature and latitude, help parse these sources of environmental and intraspecific variability; however, overemphasizing latitudinal trends can obscure the role of local environmental conditions in shaping population vulnerability to climate change. Focusing on the geographic center of a species range to disentangle latitude, we test the hypothesis that populations from warmer regions of a species range are more vulnerable to ocean warming. We conducted a mesocosm experiment and field reciprocal transplant with four populations of a marine snail, Nucella lamellosa, from two regions in British Columbia, Canada, that differ in thermal characteristics: the Central Coast, a cool region, and the Strait of Georgia, one of the warmest regions of this species' range and one that is warming faster than the Central Coast. Populations from the Strait of Georgia experienced growth reductions at contemporary summertime seawater temperatures in the laboratory and showed stark reductions in survival and growth under future seawater conditions and when outplanted at their native transplant sites. This indicates a high vulnerability to ocean warming, especially given the faster rate of ocean warming in this region. In contrast, populations from the cooler Central Coast demonstrated high performance at contemporary seawater temperatures and high growth and survival in projected future seawater temperatures and at their native outplant sites. Given their position within the geographic center of N. lamellosa's range, extirpation events in the vulnerable Strait of Georgia populations could compromise connectivity within the metapopulation and lead to gaps across this species' range. Overall, our study supports predictions that populations from warm regions of species ranges are more vulnerable to environmental warming, suggests that the Strait of Georgia and other inland or coastal seas could be focal points for climate change effects and ecological transformation, and emphasizes the importance of analyzing climate change vulnerability in the context of regional environmental data and throughout a species' range.

Forecasting parasite sharing under climate change.

Species are shifting their distributions in response to climate change. This geographic reshuffling may result in novel co-occurrences among species, which could lead to unseen biotic interactions, including the exchange of parasites between previously isolated hosts. Identifying potential new host-parasite interactions would improve forecasting of disease emergence and inform proactive disease surveillance. However, accurate predictions of future cross-species disease transmission have been hampered by the lack of a generalized approach and data availability. Here, we propose a framework to predict novel host-parasite interactions based on a combination of niche modelling of future host distributions and parasite sharing models. Using the North American ungulates as a proof of concept, we show this approach has high cross-validation accuracy in over 85% of modelled parasites and find that more than 34% of the host-parasite associations forecasted by our models have already been recorded in the literature. We discuss potential sources of uncertainty and bias that may affect our results and similar forecasting approaches, and propose pathways to generate increasingly accurate predictions. Our results indicate that forecasting parasite sharing in response to shifts in host geographic distributions allow for the identification of regions and taxa most susceptible to emergent pathogens under climate change. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Reciprocal abundance shifts of the intertidal sea stars, Evasterias troschelii and Pisaster ochraceus, following sea star wasting disease.

Disease emergence occurs within the context of ecological communities, and disease driven declines in host populations can lead to complex direct and indirect ecological effects. Varying effects of a single disease among multiple susceptible hosts could benefit relatively resistant species. Beginning in 2013, an outbreak of sea star wasting disease (SSWD) led to population declines of many sea star species along the west coast of North America. Through field surveys and laboratory experiments, we investigated how and why the relative abundances of two co-occurring sea star species, Evasterias troschelii and Pisaster ochraceus, shifted during the ongoing wasting epidemic in Burrard Inlet, British Columbia, Canada. We hypothesized that Evasterias is competitively inferior to Pisaster but more resistant to SSWD. Thus, we predicted that SSWD-induced declines of Pisaster could mitigate the negative effects of SSWD on Evasterias, as the latter would experience competitive release. We document shifts in sea star abundance from 2008-2017: Pisaster abundance and mean size declined during the outbreak, while Evasterias abundance increased from relatively rare to numerically dominant within the intertidal. When exposed to symptomatic sea stars, Pisaster and Evasterias both showed signs of SSWD, but transmission and susceptibility was lower in Evasterias. Despite diet overlap documented in our field surveys, Evasterias was not outcompeted by Pisaster in laboratory trails conducted with the relatively small Pisaster available after the outbreak. Interference competition with larger Pisaster, or prey exploitation by Pisaster during the summer when Evasterias is primarily subtidal, may explain the rarity of Evasterias prior to Pisaster declines. Our results suggest that indirect effects mediated by competition can mask some of the direct effects of disease outbreaks, and the combination of direct and indirect effects will determine the restructuring of a community after disturbance.

Host and parasite thermal ecology jointly determine the effect of climate warming on epidemic dynamics.

Host-parasite systems have intricately coupled life cycles, but each interactor can respond differently to changes in environmental variables like temperature. Although vital to predicting how parasitism will respond to climate change, thermal responses of both host and parasite in key traits affecting infection dynamics have rarely been quantified. Through temperature-controlled experiments on an ectothermic host-parasite system, we demonstrate an offset in the thermal optima for survival of infected and uninfected hosts and parasite production. We combine experimentally derived thermal performance curves with field data on seasonal host abundance and parasite prevalence to parameterize an epidemiological model and forecast the dynamical responses to plausible future climate-warming scenarios. In warming scenarios within the coastal southeastern United States, the model predicts sharp declines in parasite prevalence, with local parasite extinction occurring with as little as 2 °C warming. The northern portion of the parasite's current range could experience local increases in transmission, but assuming no thermal adaptation of the parasite, we find no evidence that the parasite will expand its range northward under warming. This work exemplifies that some host populations may experience reduced parasitism in a warming world and highlights the need to measure host and parasite thermal performance to predict infection responses to climate change.

Non-native parasite enhances susceptibility of host to native predators.

Parasites often alter host physiology and behavior, which can enhance predation risk for infected hosts. Higher consumption of parasitized prey can in turn lead to a less parasitized prey population (the healthy herd hypothesis). Loxothylacus panopaei is a non-native castrating barnacle parasite on the mud crab Eurypanopeus depressus along the Atlantic coast. Through prey choice mesocosm experiments and a field tethering experiment, we investigated whether the predatory crab Callinectes sapidus and other predators preferentially feed on E. depressus infected with L. panopaei. We found that C. sapidus preferentially consumed infected E. depressus 3 to 1 over visibly uninfected E. depressus in the mesocosm experiments. Similarly, infected E. depressus were consumed 1.2 to 1 over uninfected conspecifics in field tethering trials. We evaluated a mechanism behind this skewed prey choice, specifically whether L. panopaei affects E. depressus movement, making infected prey more vulnerable to predator attack. Counter to our expectations, infected E. depressus ran faster during laboratory trials than uninfected E. depressus, suggesting that quick movement may not decrease predation risk and seems instead to make the prey more vulnerable. Ultimately, the preferential consumption of L. panopaei-infected prey by C. sapidus highlights how interactions between organisms could affect where novel parasites are able to thrive.

Predators, environment and host characteristics influence the probability of infection by an invasive castrating parasite.

Not all hosts, communities or environments are equally hospitable for parasites. Direct and indirect interactions between parasites and their predators, competitors and the environment can influence variability in host exposure, susceptibility and subsequent infection, and these influences may vary across spatial scales. To determine the relative influences of abiotic, biotic and host characteristics on probability of infection across both local and estuary scales, we surveyed the oyster reef-dwelling mud crab Eurypanopeus depressus and its parasite Loxothylacus panopaei, an invasive castrating rhizocephalan, in a hierarchical design across >900 km of the southeastern USA. We quantified the density of hosts, predators of the parasite and host, the host's oyster reef habitat, and environmental variables that might affect the parasite either directly or indirectly on oyster reefs within 10 estuaries throughout this biogeographic range. Our analyses revealed that both between and within estuary-scale variation and host characteristics influenced L. panopaei prevalence. Several additional biotic and abiotic factors were positive predictors of infection, including predator abundance and the depth of water inundation over reefs at high tide. We demonstrate that in addition to host characteristics, biotic and abiotic community-level variables both serve as large-scale indicators of parasite dynamics.

Cyanobacterial distributions along a physico-chemical gradient in the Northeastern Pacific Ocean.

The cyanobacteria Prochlorococcus and Synechococcus are important marine primary producers. We explored their distributions and covariance along a physico-chemical gradient from coastal to open ocean waters in the Northeastern Pacific Ocean. An inter-annual pattern was delineated in the dynamic transition zone where upwelled and eastern boundary current waters mix, and two new Synechococcus clades, Eastern Pacific Clade (EPC) 1 and EPC2, were identified. By applying state-of-the-art phylogenetic analysis tools to bar-coded 16S amplicon datasets, we observed higher abundance of Prochlorococcus high-light I (HLI) and low-light I (LLI) in years when more oligotrophic water intruded farther inshore, while under stronger upwelling Synechococcus I and IV dominated. However, contributions of some cyanobacterial clades were proportionally relatively constant, e.g. Synechococcus EPC2. In addition to supporting observations that Prochlorococcus LLI thrive at higher irradiances than other LL taxa, the results suggest LLI tolerate lower temperatures than previously reported. The phylogenetic precision of our 16S rRNA gene analytical approach and depth of bar-coded sequencing also facilitated detection of clades at low abundance in unexpected places. These include Prochlorococcus at the coast and Cyanobium-related sequences offshore, although it remains unclear whether these came from resident or potentially advected cells. Our study enhances understanding of cyanobacterial distributions in an ecologically important eastern boundary system.