Ecology

Critical transition theory tells us that, as exogenous parameters drive the system towards a bifurcation and the emergence of a new equilibrium, we can see evidence of the upcoming transition through decreasing resistance to each oscillation peak15, like a ball rolling around in a cup whose walls are becoming less and less steep1,6. We find evidence of this critical slowing down within the year-to-year deceleration of rust growth rates just prior to their annual peak, or λ, our formal slowing down measure. This is coupled with a delay in the initiation month (takeoff) of the oscillation itself. The oscillations collapse in 2019 as the system apparently switches to a more benign non-epidemic state.In the mid-elevation zone of southwestern Mexico where we conducted our study, the general expectation from climate change, in addition to increased temperature, is reduced rainfall19,20, a pattern broadly in evidence for the past five years (Fig. S2). With regard to the coffee rust disease, this precipitation trend is most closely associated with the change in λ, and reflects the obligate range of associated moisture and temperature conditions required for the rust to flourish9,17. On the other hand, rust-resistant replanting has been occurring throughout coffee farms in much of Mesoamerica since the rust outbreak in 2012–201321,22. This could limit plant-to-plant spread by reducing opportunities for direct contact with an infected plant, as well as decrease the environmental spore load by reducing the contributing pool of infected plants in the broader region. On our site, the slowing down patterns of both λ and the rust takeoff point were associated with more rust-resistant replanting on a local level, while the significant linear delay in the year-to-year rust takeoff over the study period may reflect larger-scale effects emerging from increased resistance across the farm.Our preliminary treatment of April as the annual rust season initiation point corresponded generally with a seasonal pattern of increasing rainfall. This approach might be assumed by a manager experiencing the system in real time without knowledge of how the rust season will play out that year. Such an assumption works well in the first two seasons of our data, where the rust increase and rainy season both appear to begin in April. However, this association decouples in subsequent years. Evidently, the critical slowing down we initially estimated in Fig. 1B is partitioned into two components: one that imposes a lag on the initiation of the disease, and another that imposes a decelerating approach to the peak rust intensity, necessitating a joint model of the initiation month and the critical slowing down warning signal (λ). That the takeoff had a significant delaying trend over the study period suggests that the initiation of the rust season can also be seen as a measure of critical slowing down, in that a slower approach to the equilibrium point (the seasonal rust peak) will likely be reflected in a failure to even recognize the increase when it is still very small. Thus, the conspicuous change in takeoff point over time (Fig. 2A, B) itself suggests a critical slowing down and the negative values of λ in Fig. 1B may be mainly a reflection of a lag in takeoff time. The overall increasing lag in rust takeoff each year could mean that the transmission factor itself may be exhibiting a critical slowing down as the critical transition is approached, due to the progressive influence of parameters outside of the present analysis. Given the basic biology of the disease10, this trend may stem from a year-to-year secular decline in the environmental spore load causing initiation of the disease season to be deterred by a small amount each year.The evident relationship between critical slowing down and reduced rainfall is suggestive of a connection to climate change, while a slow secular increase in the proportion of rust-resistant varieties could have inhibited local or regional spread, leading to an effective “herd immunity” to the disease. The joint operation of reduced rainfall and fewer susceptible plants raises the possibility of dual bifurcations and hysteretic zones in the dynamic landscape, which we illustrate in a qualitative fashion (generalized to climate and management) in Fig. 4a. The initial outbreak, which was unexpected in light of the historically low, but persistent, levels of rust in the region7,8, was likely a critical transition precipitated by interactions between local and regional processes14. As foregrounded in Fig. 4b, we propose that a possible parameter driving the system to this initial bifurcation was recent increases in precipitation, as evidenced in local rainfall records (Fig. S2) and regional trends19. This could have propelled the system past a hysteretic phase space to where seasonal conditions dictated that the system jump to a high rust intensity equilibrium, represented conceptually in Fig. 4a by the dotted trajectory leading to the upper surface of the landscape that corresponds to an epidemic state of the rust. Likewise, in the years following the outbreak, our findings suggest that, while the system still tracked precipitation, progressive replanting of resistant varieties emerged as another parameter axis (management) that drove the system through a second critical transition back to a low rust equilibrium (Fig. 4c). Although the dynamical landscape in Fig. 4 is a qualitative representation, the trajectory along the upper surface helps to visualize how two exogenous forces, operating separately, both contributed to the critical transition we observed in our data. The trajectory we propose brings attention to the interesting possibility that the main driver of slowing down shifted from climate (precipitation) to management (replanting), leading to the second critical transition. Indeed, though the average yearly replanting rate remained roughly the same year-to-year (Fig. S1), we note that much of the cutting prior to the collapse in 2019 seemed to be concentrated in April that year (Fig. 1D), accompanied presumably by a similarly timed replanting campaign.Figure 4Envisioning the combination of climate and management effects in a joint hysteretic framing, stemming from gradual change in both forcing parameters. (A) Relative positions of rust intensity for each year are illustrated in their approximate positions with red arrows (other trajectories could be imagined based on the data presented herein). Inset plots provide a conceptualized view of the dynamics between the two forcing variables on rust intensity: (B) management (in our case, resistant variety replanting) and (C) climate (precipitation). In the inset plots, arrows indicate directions of change; solid and dashed lines indicate stable and unstable equilibria, respectively.Full size imageRecent work on critical transitions suggests that perturbances driving a system to transition are more realistically not distinct or isolated, and that the stochastic and deterministic elements of the system can therefore be entangled or even interdependent4. Likewise, we find that the variability in the environmental covariates of monthly rainfall and resistant variety replanting better explained patterns in λ than a linear trend leading up to the transition, as represented by the year variable. The correlation between the quadrat grouping offset estimates from the λ and takeoff components of the multivariate model also suggest that slowing down and delayed takeoff were associated at the individual quadrat level (Fig. 3C). Accounting for this spatial effect, these two components do not appear to be correlated by year (Fig. 3D). This suggests that the shared variability between these two indicators reflects variability in spatial environment within the plot rather than idiosyncratic effects of unique years. Besides the direct effect of resistant varieties, local stochasticity and spread dynamics may also play a role. Local growing conditions, such as variability in shade from overstory trees, can affect dispersal through rainfall splash and wind23,24. Additional management factors may also play a role, such as the vegetation structure and the presence of paths25, as well as the physical relationship between coffee plants26.Our observations of the rust dynamics themselves allow us to detect the general signals anticipating a critical transition, though the drivers may emerge from a complex system of dialectical interactions that must be considered in their whole7,27. The concept of critical slowing down thus may lend itself to application across coffee-growing regions, where predicted effects of climate change and other geographic conditions may differ9,19. Since the emergence of the rust outbreak, recommendations and protocols have been published for monitoring rust levels, potentially providing managers with regular data in changes in rust intensity for many areas9,28. As the resilience of a system can be interpreted through measuring critical slowing down prior to catastrophe2, as well as, in our case, the “exit time” from an undesirable regime4, we demonstrate that such concepts may be applied to this monitoring data to gain some insight into the system’s status. Future studies could explore signs of critical slowing down across coffee-growing regions and management systems to see how these signals predict significant changes and respond to local drivers, potentially adding to the vocabulary of agroecological management.In sum, it is clear that both a lag in takeoff point for the seasonal oscillation and the rate of approach to the peak each year seem to conspire to produce a critical slowing down, strong evidence that the decline in the disease in 2019–2020 is indeed a critical transition, regardless of the underlying mechanism. While our model suggests that two exogenous forces, rainfall and resistant variety replanting, may be driving the slowing down in our case, the underlying dynamical landscape is likely not unique to our site. More generally, the phenomenon of multivariate bifurcations leading to subsequent critical transitions (e.g., Fig. 4) is perhaps more common than thought29. Examinations of critical transitions should therefore consider the larger dynamical landscape for the possibility of subsequent transitions. More

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Species composition of stone wall treesFamilies and genera of stone wall treesThere were 96 stone wall trees belonging to 6 genera and 5 families in Macao. Among them, Moraceae and Ficus appeared the most frequently, both reaching 85 times, accounting for 88.5% (Table 1). It showed that Moraceae, a kind of tropical distribution family, was dominant in the stone wall trees communities, which meant that stone wall trees species in Macao appeared distinctly tropical nature18.Table 1 Frequency of occurrence of stone wall Trees in different families and genera.Full size tableSpecies of stone wall treesThere were 16 species of the stone wall trees in Macao including Bridelia tomentosa, Celtis sinensis, Eriobotrya japonica, Ficus altissima, F. benjamina, F. elastica, F. hispida, F. microcarpa, F. pandurata, F. subpisocarpa, F. tinctoria subsp. gibbosa, F. rumphii, F. variegata, F. virens, Leucaena leucocephala, and Trema cannabina (Fig. 2).Figure 216 species of stone wall trees in Macao (photo was taken by Professor Qin Xingsheng).Full size imageBased on the frequency of occurrence of various tree species, the frequency was concentrated in the range of 1–5%. Among them, Ficus microcarpa had the highest frequency, reaching 58 times, with a frequency of 60.4% (Fig. 3). This tree species is robust, adaptable and fast growing, which is the main population of Ficus19.Figure 3Frequency distribution of stone wall tree species in Macao.Full size imageStone wall trees in the historic center of MacaoThe historic center of Macao, covering an area of about 2.8 km2, is the heartland of Macao’s historical and cultural heritage, which plays a significant role in the cultural heritage around the world18. The historic center of Macao provides valuable historical and cultural resources that enable Macao to transform into a world tourism center20.A total of 14 plots were located in the historic Center of Macao (Fig. 4), with 45 stone wall trees, accounting for 47.9% of the total number of trees in the survey. Among them, Jardim Luís de Camões has the largest number of 9 stone wall trees. The park, built in the mid-eighteenth century, is one of the oldest gardens in Macao and has the largest number of old trees in Macao. The park had provided good time and environmental conditions for the growth of stone wall trees.Figure 4(a) Schematic diagram of distribution and number of stone wall trees in the historic Center of Macao. (b) Schematic diagram of historic center of Macao. (URL of the Macao map: https://www.d-maps.com/m/asia/china/macau/macau02.gif).Full size imageAccording to Decree No. 56/84/M of the Macao Special Administrative Region Government Printing Department, immovable property that represents the creation of man, or the development of nature or technology and has cultural significance is considered tangible cultural property. The occurrence of the stone wall tree was inextricably linked to ancient wall-building techniques of that time, which was of great significance for the study of the technological development and ecological landscape of the historic center of Macao. The concept of “historic urban landscape” was proposed by Zhang Song20, who argued that cities were organisms in continuous evolution, emphasizing respect for the interrelationship between natural and man-made environments. The stone wall trees in the historic center of Macao have been associated with the local culture and ecology tightly and should be preserved as important urban landscape.Symbiotic relationship between tree and stone wallsAs shown in the table below (Table 2), it was found that most of the stone wall trees had root systems that were not only superficially attached to the wall but also extended to the top or bottom of the wall. In particular, Ficus spp. whose strong root system could closely mosaic with the wall, thus forming a strong symbiosis.Table 2 The relationship between the root system of the stone wall tree and the wall.Full size tableStone walls can imitate the traditional nature-accommodating features to permit spontaneous establishment of a diverse plant assemblage. Besides vegetative diversities in terms of species composition, growth form and biomass structure, stone walls can support a mass collection of urban wildlife and provide various ecosystem service. It is highly recommended that modern urban design be created to embrace stone wall landscape as an integral part of naturalistic or ecological design.Vision for the establishment of the stone wall tree trail system in the historic of MacaoThe traditional street environment in the Macao Peninsula is a kind of distinctive urban landscape, which can highlight the specificity and value of the urban context. The combination of the stone wall trees and walls, together with the traditional streets, form a spatial urban landscape. Starting from the location of the stone wall tree landscape, the dots and lines are prospective to promote the establishment of a comprehensive stone wall tree landscape trail system (Fig. 5), so that the public can make use of the existing biological resources to have a better understanding of the land on which they live.Figure 5Schematic diagram of the stone wall trees trail system on the Macao Peninsula (URL of the Macao map: https://www.d-maps.com/m/asia/china/macau/macau02.gif and the finished map is created by Meisi Chen through the Photoshop CS6 and Arc GIS 10.2).Full size imageSince 2012, the Macao Government has been implementing the “Strolling along Macao Street” project, which aims at studying and exploring the history and culture of the streets of Macao through an in-depth cultural tourism route and promoting it to different levels of society. The establishment of the stone wall tree trail system can rely on this project to raise the public’s awareness of the protection and cultural identity of the stone wall tree landscape through a variety of ways. For example, route design competition, photography competition and exhibition, recruitment of “Stonewall Tree Protection Ambassadors” and other forms of participation, so that the public could complete the “role change” in the high degree of such participation—from “onlookers” to “bystanders”.Survey results of associated plant speciesSpecies composition and occurrence of frequencyThe survey showed that there were 101 species of stone wall tree associated plants in Macao, under 88 genera and 51 families. Most associated plants belonged to Euphorbiaceae, Compositae, and Araceae.There were 85 species with a frequency of 1–5 times, accounting for 84.2% of total species. A total of 11 species appeared 11–15 times, accounting for 4.0% (Fig. 6). There were a total of 4 species that appeared more than 15 times. They were Cocculus orbiculatus, Pteris cretica, Paederia scandens, and Pyrrosia adnascens. Most of the associated species appeared only 1–5 times, indicating that most plants were selective and accidental for the growth conditions of stone wall sites.Figure 6Occurrence frequency in various species of associated plants.Full size imageLife form compositionHerbaceous plants with 37 species, accounting the percentage of 52.3% (Fig. 7), were dominant in the associated plant species because the seeds of herbaceous plants are lighter and can be propagated to the wall surface by wind force.Figure 7Life form of associated plants with stone wall trees in Macao.Full size imageSimilarity analysis of the associated plants in MacaoIn order to compare the similarity of associated plant species in different environment, the surveyed sample sites for this study were divided into three categories: motorized lanes, non-motorized lanes, and park habitats (Table 3). According to Jaccard’s similarity principle, Sj is extremely dissimilar when it is 0.00–0.25, and the analysis showed that the similarity of companion plant species in all three habitats was extremely dissimilar. Therefore, it indicated that the companion plants in different habitats had obvious diversity and uniqueness.Table 3 Jaccard similarity index for companion plant species composition among three habitats.Full size table More

ALAN advances timing of activity and BMAL1 expressionDaily cycles of activity were strongly affected by the ALAN treatment (GAMM, p = 0.001, Fig. 2A and Fig. S2; Table S4). In the 5 lux group birds were generally active 6–7 h before lights-on, whereas birds in the other two light treatments (0.5 and 1.5 lux) advanced morning activity to a much lesser extent. Because of the advanced onset of activity, 40% of the overall diel activity in the 5 lux group occurred during the night, compared to 11 and 14% in the 0.5 and 1.5 lux groups, and less than 1% in the control dark group. Thus, with increasing ALAN, nocturnal activity also increased (LMM, treatment p  0.1 for pairwise comparison), and thereafter their timing remained stable. The group exposed to 5 lux showed a much larger instantaneous phase advance of almost five hours (mean ± SEM = 289 ± 21 min), and thereafter continued to gradually phase-advance until reaching a stable phase after 10 days (interaction treatment × day, p  More

OBITUARY
28 January 2022

Richard Leakey (1944–2022)

Palaeontologist of human origins, conservationist and politician.

Marta Mirazón Lahr

0

Marta Mirazón Lahr

Marta Mirazón Lahr is professor of human evolutionary biology and prehistory at the University of Cambridge, UK. Leakey was a friend, colleague and supporter of her work in Turkana, where she directs research in human origins.

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Richard Leakey made palaeontological discoveries of lasting significance, and brought animal poaching to the world’s attention. His fossil finds at Koobi Fora on the shores of Lake Turkana, Kenya, transformed our understanding of the diversity of human ancestors. He directed Kenya’s national museum, reorganized the country’s wildlife services and headed Kenya’s civil service. He died aged 77, at home in the Ngong Hills, Kenya.In science, he liked exploration, big-picture problems and building institutions. He made huge strides in conservation, empowering organizations and deploying shock tactics. He entered politics, creating an opposition party, then worked in government, finally becoming its corruption watchdog. He mentored young Kenyan scholars, conservationists and artists who are now leaders in their field.Born in Nairobi, Richard was the middle child of pioneers in African palaeontology and archaeology Louis and Mary Leakey. He abandoned school at 16 to open an animal-trapping and safari business, earning enough to pay for flying lessons and his own small plane. In 1963, a mix of interest in his parents’ world and a wish to prove himself to them lured him into the study of the past, and he found his first important hominin fossil — a 1.5 million-year-old mandible of Paranthropus boisei — in 1964.
Fifty years after Homo habilis
In 1967, Leakey’s father asked him to direct an expedition to the Omo Valley of southern Ethiopia. There, Leakey found two Homo sapiens fossils now known to be 230,000 years old (C. M. Vidal et al. Nature https://doi.org/gn3794; 2022), key evidence of our species’ African origins. Flying over the eastern shore of Lake Turkana, he recognized the potential of sediments at Koobi Fora, which proved to be a trove of hominin fossils. The discovery of different hominin species living at the same time between 2 million and 1.5 million years ago (P. boisei, Homo habilis, Homo rudolfensis and Homo erectus) changed views of how humans evolved.In 1968, Leakey became director of the National Museums of Kenya, which became a hub of thriving research. Soon afterwards, he met the young British zoologist Meave Epps. They married after his first marriage ended, and became life-long personal and scientific partners. Their work with researchers dubbed the Hominid Gang, led by Kamoya Kimeu, resulted in the discovery of dozens of hominin fossils, including a new genus and four new species (Paranthropus aethiopicus, Australopithecus anamensis and Kenyanthropus platyops, as well as H. rudolfensis). A 1.6-million-year-old skeleton of a juvenile H. erectus proved to have grown more slowly than apes and faster than humans, giving insights into the evolution of human life-history.Leakey became involved in acrimonious scientific arguments — sometimes he was right, sometimes not — which, during the 1970s, gave an antagonistic tone to human-origins research. His health deteriorated, and he had his first kidney transplant (donated by his brother Philip) in 1980. In 1989, Kenya’s president, Daniel arap Moi, asked him to run the Kenya Wildlife Service (KWS). Leakey declared war on poachers, burnt the stockpile of Kenyan ivory and massively reduced elephant deaths. His controversial tactics had an impact on a web of corrupt practices and created serious enemies. In 1993, the plane he was piloting crashed; both his legs had to be amputated below the knee. Sabotage was rumoured.
Human evolution’s ties to tectonics
The relationship with Moi became increasingly hostile. In 1995, Leakey left KWS to create an opposition party, Safina, becoming a member of the Kenyan parliament in 1998. His time in opposition was tense. Leakey was beaten and received death threats. But Kenya needed large investments, and funders demanded assurances. Capitalizing on Leakey’s reputation for integrity, in 1998 Moi asked him to direct KWS again, and in 1999 to head the civil service. Over three years, Leakey raised hundreds of millions of dollars for Kenya and fought corruption.In 2002, he accepted a position at Stony Brook University, New York, that allowed him to live in Kenya and create the Turkana Basin Institute (TBI), which he chaired from 2005 until his death. TBI fostered a burst of discoveries: Miocene primates, hominins, the oldest stone tools in the world at 3.3 million years, evidence of prehistoric warfare, and the earliest monumental architecture in sub-Saharan Africa. In 2004, Leakey founded WildlifeDirect, a non-governmental conservation body, serving on its board for 10 years. In 2007, he became chair of Transparency International Kenya, continuing his battle against corruption.By this time, Leakey had skin cancer and progressively worse health. He underwent a second kidney transplant in 2006, with Meave as the donor, and a liver transplant in 2013. Yet, in 2015, he accepted President Uhuru Kenyatta’s request to return to KWS as chair until 2018. For the past six years, he worked to create a new Kenyan museum, called Ngaren — of which I am a board member — to celebrate science, evolution and humanity’s African origins.Richard was special — fun, insightful, generous, with a sharp sense of humour, and a fabulous cook and sommelier. He embraced life, good and bad, and imbued those around him with the sheer excitement of what could be done, discovered, resolved and enjoyed.

Nature 602, 29 (2022)
doi: https://doi.org/10.1038/d41586-022-00211-6

Competing Interests
M.M.L. is a member of the board of directors of Ngaren, a non-governmental organization founded by Richard Leakey to support the creation of a museum of evolution in Kenya.

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