Biodiversity baselines: Tracking insects in Kruger National Park with DNA barcodes

Biodiversity baselines: Tracking insects in Kruger National Park with DNA barcodes

Philile Dlamini, Woodlands section ranger, Kruger National Park. PHOTO CREDIT: Hannah James

Biodiversity baselines: Tracking insects in Kruger National Park with DNA barcodes

A video abstract for the Kruger Malaise Program publication

March 24, 2021

By Michelle Lynn D’Souza

One year, 25 Malaise traps, and the dedication of numerous park rangers and staff have led to valuable insights and resources for Kruger National Park, South Africa.

This video abstract highlights work that involved the analysis of 367,743 insect specimens collected at 25 sites in Kruger National Park (KNP) in South Africa and it revealed 19,730 species, a count equal to 43% of the known insect diversity in Southern Africa. Species assemblages were differentiated between ecoregions and were structured most strongly by variation in rainfall. These efforts have delivered the baseline data needed to assess future changecomprehensive, spatially and seasonally explicit data on insect biodiversity in KNP.

The next steps involve extending the analysis to other national parks in South Africa, and ultimately, to the world’s 4000 national parks. The aim is to obtain the baseline data required to assess insect communities and usher in the global biomonitoring systems needed to aid scientists and citizens in forecasting changes in biodiversity.

For full details, please refer to the publication in Biological Conservation.

For more information on the program efforts, see: Kruger Malaise Program summary

I and the co-authors of the publicationMichelle van der Bank, Zandisile Shongwe, Ryan D. Rattray, Ross Stewart, Johandré van Rooyen, Danny Govender, and Paul D. N. Hebert—wish to acknowledge the contributions of staff and rangers in Kruger National Park for making the collections. We also thank the staff at South African National Parks for providing research permits and access to metadata as well as logistic support. We thank staff and students at the African Centre for DNA Barcoding in Johannesburg and at the Centre for Biodiversity Genomics in Guelph for aid in collecting, shipping, sorting, sequencing, and imaging specimens along with all funding sources.

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Also in BIOSCAN

HOW A TROPICAL COUNTRY CAN DNA BARCODE ITSELF

by Dan Janzen and Winnie Hallwachs | Oct 2, 2019

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Using DNA barcodes in the fight against Malaria

Using DNA barcodes in the fight against Malaria

Using DNA barcodes in the fight against Malaria

Researchers in Ghana along with Target Malaria, the University of Oxford and the Centre for Biodiversity Genomics work to uncover the role of the Anopheles gambiae mosquito.

January 27, 2021

By Michelle Lynn D’Souza

Target Malaria aims to reduce malaria transmission by reducing the population of malaria-transmitting mosquitoes using genetic technologies. As part of their research, they want to know the ecological implications of reducing populations of the mosquito—the key vector for malaria in Africa.

Researchers are using DNA barcoding technologies to catalogue the insect community in Ghana. They will then use this catalogue or library to identify the insect species that are eaten by local birds, bats, and other insect-eating arthropods as well the host species in a mosquito bloodmeal, all through metabarcoding techniques that identify DNA fragments by matching sequences to the local DNA barcode library.

In the end, they will use these data to construct an ecological network that will quantitatively demonstrate how Anopheles gambiae is connected to the other members of the ecosystem.

These efforts are a demonstration of the power of DNA barcoding and its ability to reveal the nature and intensity of interactions among all species. This endeavour, to reveal species interactions to clarify their role in structing biological communities, is a key research theme of BIOSCAN, iBOL’s new seven-year, $180 million global research program that aims to revolutionize our understanding of biodiversity and our capacity to manage it.

For more information on Target malaria efforts in Ghana see: The important interactions behind the itch

For more information on BIOSCAN see:  BIOSCAN – Illuminating biodiversity and supporting sustainability

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HOW A TROPICAL COUNTRY CAN DNA BARCODE ITSELF

by Dan Janzen and Winnie Hallwachs | Oct 2, 2019

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The important interactions behind the itch

The important interactions behind the itch

The important interactions behind the itch

The potential consequences of reducing Anopheles gambiae mosquitoes to control Malaria

Ghanaian researchers sorting insect samples at the University of Ghana, Accra, Ghana.

IMAGE CREDIT: Michelle L. D’Souza; PHOTO CREDIT: Lema Concepts Africa

Written by

Talya D. Hackett

Talya D. Hackett

Department of Zoology, University of Oxford, Oxford 

Karen E. Logan

Karen E. Logan

Target Malaria, Dept Life Sciences, Imperial College London, UK

Michelle L. D'Souza

Michelle L. D'Souza

Centre for Biodiversity Genomics, University of Guelph, Guelph, CA

January 27, 2021

doi:10.21083/ibol.v11i1.6267

Only four months after China reported its first COVID-19 case to the World Health Organization (WHO) the virus had spread to every nation on the African continent. Despite being home to 17% of the world’s population, Africa currently accounts for just 2.5% of COVID-19 related deaths1. But the pandemic may well have caused many more to die, not from coronavirus, but from malaria.

The 2020 World Malaria Report warned that disruptions to malaria prevention and treatment caused by the coronavirus could see as many as 100,000 malaria-related deaths in Sub-Saharan Africa2. Similar effects were unfortunately experienced during the 2014-2015 outbreaks of Ebola in West Africa3. While most strategies being employed to control malaria have worked well, progress to reduce its incidence has stagnated. New strategies are needed to prevent the mortality rate from increasing further and to better prepare countries in the face of other unexpected pressures.

With the ambitious goal to create a world free of malaria, one not-for-profit research consortium–Target Malaria–is developing novel technologies using genetic modification to control the numbers of the malaria-transmitting mosquitoes.

The nature of malaria and the microbe responsible

Malaria is a disease that starts with a small single-celled parasite. This microorganism belongs to the genus Plasmodium, and of the four species that threaten humans, P. falciparum and P. vivax are the most common, and the former the most dangerous4.

Female mosquitoes alone spread malaria in nature. An infected mosquito injects a small number of parasites into its victim’s bloodstream while it feeds, and the parasites then travel to the liver where they multiply rapidly before infecting red blood cells. Flu-like symptoms begin when the parasites break out of the blood cells, one to four weeks after the bite.

Of the 229 million confirmed malaria cases worldwide in 2019, 94% occurred in Africa2. Even more devastating, of the 409,000 malaria-associated deaths, 84% occurred in children under the age of five.

While there are more than 3,500 species of mosquito worldwide and 837 in Africa, three very closely related species are responsible for most transmission of the disease: Anopheles gambiae, Anopheles coluzzii, and Anopheles arabiensis. These three species belong to the Anopheles gambiae complex which, if targeted, is likely to have the largest effect on the transmission of malaria. This species complex has tightly evolved with humans and is the key vector for malaria in sub-Saharan Africa.

Current vector control tools such as insecticides, bed nets, and drugs have been effective in reducing malaria cases but not in eradicating the disease. Target Malaria’s approach is meant to be complementary to the existing interventions by focusing on malaria control by mosquito control.

Researchers unify under Target Malaria

In 2003, Prof. Austin Burt published a seminal paper5 describing the principle of genetically modifying a population of mosquitoes for applications in the control of vector-borne diseases. Prof. Burt predicted that malaria-transmitting mosquitoes could potentially disappear in an area within two years when using these novel genetic tools. It was fortuitous that only a few years prior in Imperial College London, where Prof. Burt was working, a team lead by Prof. Andrea Crisanti had created the first reliable system for germline transformation of a malaria-transmitting mosquito6.

The two groups were brought together in 2005 with a grant given as part of the Grand Challenges in Global Health initiative and in a little over a decade the team’s scientific progress had resulted in a new mechanism for genetic control measures within An. gambiae7.

The initial group of researchers has now grown into a team of 180 project members, with collaborating research partners in Africa, Europe, and North America. As the work progressed, the project grew under its new brand–Target Malaria.

Target Malaria is working with five African partner sites.
IMAGE CREDIT: Michelle L. D’Souza

Today, Target Malaria is working with five African partner sites: Burkina Faso, Cape Verde, Ghana, Mali, and Uganda. This work is being headed by Dr. Abdoulaye Diabate at the Institut de Recherche en Sciences de la Santé (Research Institute on Health Sciences), Bobo-Dioulasso, Burkina Faso; Dr. Adilson de Pina at the Instituto Nacional da Saude (National Institute of Public Health, CCS-SIDA), Cape Verde; Dr. Fred Aboagye-Antwi at the University of Ghana, Accra, Ghana; Dr. Mamadou Coulibaly at the University of Bamako Malaria Research and Training Center, Bamako, Mali; and Dr. Jonathan Kayondo at the Uganda Virus Research Institute, Entebbe, Uganda.

Each of the African partners and their teams bring a different skillset to the collaboration, none being able to deliver all key elements independently. A relationship of co-development is fostered within the project with scientists working together across countries and with communities towards a common objective and vision–a world free of malaria.

The three key guiding pillars

Target Malaria’s work is structured around three key pillars: science, stakeholder engagement, and regulatory affairs. Each pillar is essential for the project’s success, supporting responsible research and development of genetic technologies, a commitment to engaging a wide variety of stakeholders, as well as ensuring compliance with all national regulations and laws. 

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Science

To date, Target Malaria has made significant scientific advancements on the path to developing a new tool for vector control for malaria. Researchers have demonstrated the proof of concept in creation of a transgenic sterile male An. gambiae8 strain, demonstration of the ability to modify a laboratory population of An. gambiae mosquitoes to be male biased9, suppression of a small cage population of laboratory reared An. gambiae mosquitoes10, creation of the first gene drive mosquitoes capable of suppressing a laboratory population of An. gambiae mosquitoes11, modelling the potential of genetic control of malaria mosquitoes12, modelling suppression of malaria vector using gene drive13, and the importation of the first genetically modified mosquitoes (a self-limiting sterile male line) into Burkina Faso for contained laboratory use in 2016 and regulatory approval for the subsequent release of the same self-limiting sterile male line in 2019.

Stakeholder engagement

The list of stakeholders is vast, from grass roots, those local communities where the project is working, through to local civil society organizations, regional governing bodies, and the appropriate governmental agencies, all in-country, as well as a range of interested parties outside of the African partner countries. Target Malaria is committed to ensuring that the stakeholders understand the research and long-term goals of the project enabling them to make an informed decision on whether to support the project’s efforts. Engagement also helps ensure that the research is welcomed and useful in the fight against malaria. Most importantly, Target Malaria will learn a lot from their stakeholders through the process.

Regulatory affairs

While an important aspect of Target Malaria’s strategy is to focus on the communities that might benefit from the technology and that are most concerned by the research activities, they also have an ongoing, transparent dialogue with other stakeholders at the national and international level. For example, the project is taking a phased approach to its development pathway in line with guidance from the WHO14.

Technology being developed

The goal is to develop modified mosquitoes that can pass on to their progeny a self-sustaining genetic change, a process aiming to reduce specific mosquito populations to break the malaria transmission cycle. To do so, Target Malaria is using gene drive, a phenomenon that occurs in nature and causes a selected trait to rapidly increase in frequency through a population via sexual reproduction over several generations. Gene drive works by increasing the likelihood–from the usual 50 per cent to greater than 95 per cent–that a modified gene will be inherited by its offspring. This means that over the course of several generations, a selected trait could become increasingly common within a specific species (depending on the specific area and how the animals move around within it).

Researchers are investigating the use of genes that produce enzymes that cut specific sequences of DNA. Called nucleases, these enzymes found in simple single celled organisms can copy themselves from one chromosome to another5. When introduced into the malaria mosquito, the nuclease works by identifying and cutting a selected site within essential genes targeted by researchers, rendering them functionless, such as reproductive genes. The subsequent effects depend on the nature and importance of the gene.

Target Malaria’s goal is to produce modified malaria mosquitoes that can pass these genes on to greater than 95 per cent of their offspring, so the modification is spread throughout the specific population relatively quickly and is effectively “self-sustaining”. This strategy is known as population suppression, and as the mosquitoes themselves do the work of spreading the modification, it makes the reduction of the malaria mosquito population relatively cost effective and simple to implement.

Current gene drive research is at an early stage, and so definitive decisions about gene drive-based tools are premature. Based on current progress, field releases of a gene drive-based tool are many years away. This gives scientists and stakeholders, specifically those from countries where gene drives might one day be employed, valuable time to consider the important questions of regulation, risk assessment, ethics, and engagement, and to prepare for assessing any application related to gene drive mosquitoes and their potential use as a tool for vector control for malaria.

An ecological approach spearheaded in Ghana

As the gene drive approach in development by Target Malaria will specifically target the An. gambiae complex to reduce its population, it is vital to ensure there are no undesirable consequences to the rest of the plant and animal communities. In Ghana, researchers are focusing on the ecological implications of the work; the role of the An. gambiae mosquito in the broader ecosystem. The ongoing research in Ghana aims to predict these potential effects.

 

Researchers setting off to sample the insect community around a Ghanaian village.

PHOTO CREDIT: Michelle L. D’Souza

THE ECOLOGICAL ROLE OF MOSQUITO LARVAE IN AQUATIC ENVIRONMENTS

read more…

WHAT WE KNOW, DON’T KNOW, AND THINK WE KNOW ABOUT THE PREDATORS OF MOSQUITOES

read more…

POLLINATORS OR NECTAR THIEVES? THE ROLE OF MALARIA-TRANSMITTING MOSQUITOES IN POLLINATION

read more…

ECOLOGICAL AND EPIDEMIOLOGICAL INSIGHTS FROM BLOOD MEALS

read more…

While some aspects of An. gambiae ecology is well studied, research in Ghana will provide a more complete picture, specifically determining the interactions between An. gambiae and other mosquito species as well as predators, prey, and vertebrate hosts. In this sense, the research is based on a community ecology approach rather than looking at just mosquito ecology.

Researchers are sampling, as far as they are able, insects from the entire aerial communities across all habitats, not just where they expect to find high numbers of An. gambiae. Equally true for insectivores that might feed on mosquitoes or similar small aerial insects, they are taking fecal samples or stomach contents. In aquatic habitats, they are sampling from a range of water bodies and collecting representatives across all insect and insectivorous groups. And, because adult mosquitoes rely on flower nectar for food, they are sampling the pollinator community as well. Finally, they are looking at the community of biting flies and their vertebrate hosts by determining blood-meal interactions to better understand shared hosts and the potential for zoonotic disease transmission15. Importantly, all methods and target sample numbers have been cleared by independent ethics boards at both the University of Ghana and the University of Oxford to ensure there is no lasting impact on the community of plants and animals where the work takes place.

Insect samples collected around a Ghanaian village using Malaise traps (top) before being sorted and pinned (bottom) at the University of Ghana.
PHOTO CREDIT: Lema Concepts Africa

Using this broad community approach allows researchers not only to describe the role of An. gambiae in the ecosystem but also to predict how the rest of the ecological community would respond to An. gambiae reduction. For example, the data would allow them to determine which insects might face more pressure from predators if those that feed on mosquitoes shifted their feeding behaviour to replace An. gambiae in their diet and how this change might affect the rest of the food web. As there is no known animal or plant that relies solely on An. gambiae16, and food webs tend to rewire following minor perturbations17,18, it is predicted that there will not be any significant effects because of An. gambiae population reduction. Regardless, it is necessary to ensure this is the case and a community ecology approach will make this possible.

Some of the faces of the research team in Ghana. Dr. Fred Aboagye-Antwi (Ghanaian Principle Investigator, top left), Helen Selorm Wohoyie (Assistant Stakeholder Engagement and Communications Advisor, top center), Divine Dzokoto (Senior Stakeholder Engagement and Communications Advisor, top right) and Dr. Talya D. Hackett (project coordinator), Bernard Aiye Adams, Ezekiel Yaw Donkor, and Naa Na Afua Acquaah (laboratory technicians) (bottom, left to right).
PHOTO CREDIT: Lema Concepts Africa

Building a DNA barcode reference library for Ghana

The tools being used to construct the food web are mostly molecular-based, all requiring the creation of a DNA barcode library for insects in the area as the important first step. To this end, researchers in Ghana regularly collected terrestrial insects from villages in the southeast of Ghana for a year.

Once the library is established, they can then start looking at the feces and the gut contents of insectivores and use that library to match and identify prey DNA fragments using DNA metabarcoding.

Researchers are using a similar metabarcoding approach for the aquatic food web while for the pollination network they will use a combination of traditional observational methods and DNA metabarcoding of pollen from caught insects. Finally, for the blood meal analysis, they are metabarcoding the blood meals of fed mosquitoes and other biting flies to identify what has been bitten.

The ecological research in Ghana is a collaboration between Dr. Fred Aboagye-Antwi at the University of Ghana, Prof. Sir Charles Godfray and Prof. Owen Lewis at the University of Oxford, as well as an extensive team of postdoctoral researchers, Ph.D. students, and technicians at both institutions. Part of the UK team, postdoctoral researcher and project coordinator, Dr. Talya D. Hackett is organizing efforts between countries, including a collaboration with the Centre for Biodiversity Genomics (CBG) in Guelph, Canada, global leader in the field of DNA barcoding. Supported by Prof. Paul D. N. Hebert, the Director of CBG, and Dr. Michelle L. D’Souza, samples from Ghana have begun making their way to the large sequencing platforms housed at the CBG.

Dr. Talya D. Hackett (left) and Dr. Michelle L. D’Souza (right) discuss DNA barcode data compatibility across platforms EarthCape and BOLD Systems at the University of Ghana.
PHOTO CREDIT: Lema Concepts Africa

So far, about 3,000 insects have been processed and 530 BINs (species proxies) have been documented, about 70% of which are unique to the project. Efforts will ultimately barcode 100,000 specimens and fill a large gap in barcode data currently missing from West Africa.

Conclusions

Examining diets to determine species-specific interactions in a complex community food web is only possible at this large scale with molecular techniques, and only recently, because the costs of DNA barcoding and metabarcoding techniques have dropped. Even five years ago this sort of a project would not have been feasible.

Apart from building large, comprehensive food webs, these data can further inform our understanding of things like community structure and insect abundances across time and space, the dietary overlap of insectivorous species, and niche overlap of different mosquito species.

All data will be made publicly available. Ultimately, this project is creating a wealth of information, not just for Target Malaria’s research goals, but for the broader scientific community and for other people within Ghana and West Africa.

These efforts are a demonstration of the power of DNA barcoding and its ability to reveal the nature and intensity of interactions among all species. This endeavour, to reveal species interactions to clarify their role in structuring biological communities, is a key research theme of BIOSCAN, iBOL’s new seven-year, $180 million global research program that aims to revolutionize our understanding of biodiversity and our capacity to manage it.

If you would like to know more about Target Malaria, go to www.targetmalaria.org

References:

1. World Health Organization (2020) WHO Coronavirus Disease (COVID-19) Dashboard. Accessible at: https://covid19.who.int/

2. World Health Organization (2020) World malaria report. Accessible at: https://www.who.int/teams/global-malaria-programme/reports/world-malaria-report-2020

3. Wang J et al. (2020) Preparedness is essential for malaria-endemic regions during the COVID-19 pandemic. The Lancet 395(10230), 1094–1096. doi: 10.1016/s0140-6736(20)30561-4

4. Crutcher JM, Hoffman SL. Malaria. In: Baron S, editor. Medical Microbiology. 4th edition. Galveston (TX): University of Texas Medical Branch at Galveston; 1996. Chapter 83.

5. Burt A (2003) Site-specific selfish genes as tools for the control and genetic engineering of natural populations. R. Soc. London. Ser. B Biol. Sci. 270:921–928. doi: 10.1098/rspb.2002.2319

6. Catteruccia F, Nolan T, Loukeris TG, Blass C, Savakis C, Kafatos FC, Crisanti A (2000) Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405(6789):959-962. doi: 10.1038/35016096.

7. Windbichler N, Menichelli M, Papathanos PA, Thyme SB, Li H, Ulge UY, Hovde BT, Baker D, Monnat RJ Jr, Burt A, Crisanti A. (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature. 473(7346):212-215. doi: 10.1038/nature09937.

8. Windbichler N, Papathanos PA, Catteruccia F, Ranson H, Burt A, Crisanti A (2007) Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucleic Acids Res. 35(17):5922-5933. doi:10.1093/nar/gkm632

9. Galizi R, Doyle LA, Menichelli M, Bernardini F, Deredec A, Burt A, et al. (2014) A synthetic sex ratio distortion system for the control of the human malaria mosquito. Commun., 5: 1–8.

10. Hammond AM, Kyrou K, Bruttini M, North A, Galizi R, Karlsson X, et al. (2017). The creation and selection of mutations resistant to a gene drive over multiple generations in the malaria mosquito. PLOS Genet. 13:e1007039.

11. Kyrou K, Hammond AM, Galizi R, Kranjc N, Burt A, Beaghton AK, et al. (2018) A CRISPR–Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Biotechnol. 36:1062–1071

12. North AR, Burt A & Godfray HCJ (2019) Modelling the potential of genetic control of malaria mosquitoes at national scale. BMC Biol. 17: 26.

13. North AR, Burt A & Godfray HCJ (2020) Modelling the suppression of a malaria vector using a CRISPR-Cas9 gene drive to reduce female fertility. BMC Biol. 18:98.

14. World Health Organization (2014) Guidance framework for testing of genetically modified mosquitoes. Accessible at: https://www.who.int/tdr/publications/year/2014/en/

15. Bellekom B, Hackett TD & Lewis OT (2021) A Network Perspective on the Vectoring of Human Disease. Trends Parasitol.

16. Collins CM, Bonds JAS, Quinlan MM & Mumford JD (2018) Effects of the removal or reduction in density of the malaria mosquito, Anopheles gambiae s.l., on interacting predators and competitors in local ecosystems. Vet. Entomol. 33(1):1–15. doi: 10.1111/mve.12327

17. Timóteo S, Ramos JA, Vaughan IP & Memmott J (2016) High resilience of seed dispersal webs highlighted by the experimental removal of the dominant disperser. Biol. 26:910–915. doi: 0.1016/j.cub.2016.01.046

18. Bartley TJ, McCann KS, Bieg C, Cazelles K, Granados M, Guzzo MM, et al. (2019) Food web rewiring in a changing world. Ecol. Evol. 3: 345–354. doi: 10.1038/s41559-018-0772-3

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30 million reasons you will be missed

30 million reasons you will be missed

30 million reasons you will be missed

Pioneer field biologist, entomologist, and mentor, Terry Erwin passes away at age 79
Erwin supervising the trees at work, the Tiputini Research Station, Ecuador, 2013. PHOTO CREDIT: Beulah Garner

The world lost a brilliant mind last week when Terry L. Erwin passed away on May 11, 2020, at the age of 79. Many among us in the scientific community feel this great loss, for you did not need to have personally known, or even have met Erwin to recognize the name or appreciate the significance of his work.

    Erwin not only published prolifically on beetle systematics – describing four tribes, 22 genera, and 439 species of Carabidae – but also tremendously influenced the way many think about biodiversity.

    “He brought alive for many the far-off world and the mysteries therein of the neotropics,” said Beulah Garner, Senior Curator at the Natural History Museum in London, and Erwin’s colleague and friend of nine years. “I think it was the first time anyone, through their scientific exploration, had made a place and a fauna at once seem magical, touchable, and quantifiable.”

    Erwin was serving as a research entomologist and curator of Coleoptera at the Smithsonian Institution’s National Museum of Natural History at the time of his death. He was a pioneer in neotropical conservation biology and canopy research, having developed the study of tree canopy insects into an academic discipline as early as 1974.

    Notably, in his small paper in 1982 that examined canopy beetles and host plant relationships to understand the number of species present in an acre of Panamanian forest, Erwin dramatically expanded our conception of terrestrial insect diversity.

    Graphical abstract of Erwin’s 1982 paper IMAGE CREDIT: Michelle Lynn D’Souza

    As a young graduate student interested in using DNA barcoding to evaluate insect diversity in Central America and to assess global diversity estimates, Erwin’s work was a guidepost for my own research. His 1982 publication was particularly iconic. Ironically, it was in the last ‘throwaway’ paragraph (as he described it) – suggesting the presence of 30 million arthropod species, at the time estimated to be around one-and-a half million – that he sparked a global debate about the number of species on the planet.

    Even years later, he was enduring in his defense of the ‘30 million’ estimate, according to Garner. His holistic approach to field biology, with Carabidae at its core, enabled him to understand the relatedness of species as well as the mechanisms that drive such incredible diversity so clearly. “Even higher [than 30 million] he would say! And, having been in the field with him, with his meticulous observations of the microverse, his pioneering investigations into the forest canopy, I absolutely believe him,” said Garner. “These were not assumptions from a dataset, a modelling outcome, these were from direct in-field observations: a true naturalist.” While his estimate has been debated, refuted, and revised to approximately seven million arthropod species, the discussion remains active today.

    A true naturalist at home in the jungles of Yasuni National Park, Ecuador, 2018.
    PHOTO CREDIT: Beulah Garner

    While always having been interested in DNA-based techniques, it was not until much later in Erwin’s career that he used it in his own work. Heavily involved in the field of systematics, he was among the first of those in the early 1980s that experienced its infusion with the beginnings of gene sequencing. While in its own right revolutionary, sequencing technology was just another tool to study the natural world, one that would eventually be replaced by the tricorder, Erwin explained to Dr. Bilgenur Baloglu, then a Ph.D. student at the National University of Singapore studying chironomid diversity, in an interview during the International Congress of Entomology in Florida in 2016. He was referring to DNA barcoding and the beginnings of Drs. Paul Hebert and Dan Janzen’s tests with Costa Rican moths.

    As noted by Dr. Scott Miller, science committee member of the International Barcode of Life Consortium (iBOL) and deputy undersecretary at the Smithsonian Institution, Erwin was always enthusiastic about collaborations between iBOL and the Smithsonian to barcode insect genera, such as that currently funded by the Global Genome Initiative (GGI). He is the main reason that Carabid beetles were one of the first families covered under the project, contributing substantially to the species barcoded and deposited on the Barcode of Life Data Systems (BOLD), according to Miller. He also collaborated with Dr. Carlos Garcia-Robledo and others at the Smithsonian on a series of papers on insect-host plant relationships, among many others, that used DNA barcoding to identify the gut contents of insect herbivores as well as egg and larval plant associations to reconstruct species interactions in tropical networks.

    Miller first began working with Erwin in 1986 at the Smithsonian Institution as a postdoctoral fellow. Together they had a vision that became the Biodiversity in Latin America Tropics (BIOLAT), a program based around standardized sampling, something that may seem logical now, but was novel in fields like entomology at the time, according to Miller. Since then, a lot of other organizations have tried similar standardized programs but have struggled under the weight of the taxonomic impediment.  “When seen against this background, iBOL initiatives such as the Global Malaise Program or BioAlfa are truly amazing,” said Miller. “It is most unfortunate that DNA barcoding was not available when Terry started canopy fogging!”

    Erwin canopy fogging at 4 a.m. at the Onkone Gare camp, Yasuni National Park, Ecuador, 2018.
    PHOTO CREDIT: Beulah Garner

    From planning BIOLAT, to consulting for Biosphere 2 (the subject of the documentary ‘Spaceship Earth’), to the initial canopy fogging endeavour in Papua New Guinea (PNG) that eventually led to the Binatang Research Center and the PNG insect ecology program, Erwin encouraged, guided, and inspired Miller’s endeavours for years.

    Terry understood the importance of nurturing the next generation of talent, and especially the importance of diversifying the [scientific] pipeline.

    Dr. Scott Miller

    Science committee member of the International Barcode of Life Consortium (iBOL) and deputy undersecretary at the Smithsonian Institution

    “Terry understood the importance of nurturing the next generation of talent, and especially the importance of diversifying the [scientific] pipeline,” says Miller. “Terry was always eager to provide opportunities for young scientists, especially women, and people from developing countries.” While working together at the Smithsonian, Miller recounts how Erwin always hosted interns and fellows, bringing them to meetings and conferences, and trying to connect them to future opportunities.

    Erwin had the greatest spirit of academic generosity, quick to provide advice, a reference from his encyclopedic library, or specimens for one’s own research, according to Garner. Erwin nurtured a passion for discovery in many students and inspired it in even more biologists. As he told Bilgenur back in 2016, you do not become a biologist if you are out for money, but you do it for the joy of being out in the field. “For me, the bottom line is if you like fieldwork, be a biologist. It’s the best place to be,” said Erwin in her interview. “If you are out in the rainforest, every single day, actually maybe every hour, there’s a tremendous discovery. And that’s what’s really rewarding – discovery.”

    Erwin hunting Carabidae near the Tiputini Research Station, Ecuador, 2013.
    PHOTO CREDIT: Beulah Garner

    In the field, Garner recounts, Erwin would wake early, sit by the Tiputini river with black coffee and binoculars, and study the jungle whilst it woke. “Canopy fogging is a race to finish before the dawn and Terry was indefatigable,” said Garner. “It’s 4 a.m. in the primary jungles of South America, you’re setting up your traps, and Terry is right beside you, overseeing operations as if the rainforest were his orchestra and he the conductor.” In the evening after supper with head torch and aspirator, it would be time to go on a Carabidae hunt.

    It’s 4 a.m. in the primary jungles of South America, you’re setting up your traps, and Terry is right beside you, overseeing operations, as if the rainforest were his orchestra and he the conductor.

    Beulah Garner

    Senior Curator at the Natural History Museum, London

    He was fearless, saving Garner from a pack of marauding peccaries in Ecuador, as well as rescuing her from bivouacking army ants as they surrounded their camp in the dead of night. “He was and is the reason I endeavour to be a good field biologist,” said Garner. “His compassion and consideration and genuine every-day awe for the natural world is a method to live and work by.”

    Beulah Garner (left) and Terry Erwin (right) inspecting the flight intercept traps, Tiputini Research Station, Ecuador, 2013. PHOTO CREDIT: Dr. Kelly Swing

    Erwin very much valued the natural world, possessing an astute understanding of it that unfortunately, he takes with him. He feared having species reduced to just a sequence and believed that the rich natural history and the awe that the living world inspires in us needed to be accounted for as well, sentiments that led him to catalyze the Encyclopedia of Life (EOL) in 2004, according to Nana Naisbitt, EOL co-catalyst, founder of Chalkboard, and Erwin’s dear friend of 22 years. The EOL makes knowledge about life on Earth globally accessible and has had a long-standing collaboration with BOLD.

    As Naisbitt explained, Erwin was a profound mentor, one who changed the course of her life and the lives of many others through her work and her connection to him. He effectively snowballed Naisbitt’s career as a science champion, instrumental in her founding the Pinhead Institute, a science education non-profit and Smithsonian Affiliate. He was also key to many community outreach and mentorship programs while she worked as Executive Director of the Telluride Science Research Center, a job she got because of her work as the director of Pinhead. “It’s just impossible to say how many people he impacted,” said Naisbitt. “Terry liked to say that he plants seeds – ideas in students – and watches them grow. He planted countless seeds that grew strong and bright.”

    In Naisbitt’s assessment, Erwin was able to help so many people flourish because he possessed a phenomenal gift in the way he supported them and gave them confidence without being intrusive. “He connected me to the right people, then showed up for and supported me. Most times he would just sit there quietly in meetings and let me do the talking,” said Naisbitt. “His reputation and presence were enough – it conveyed the message, ‘I anoint this person’. In that way, he was so unbelievably respectful.”

    Naisbitt said that she had the impression Erwin believed he stood on the shoulders of giants. She described to me this image she had of him, of someone reaching down and pulling up younger scientists to stand on his shoulders. “And he did that so well. He did it over and over again, with immense generosity and without ego. And that is so rare.”

    His reputation and presence were enough – it conveyed the message, ‘I anoint this person’. In that way, he was so unbelievably respectful.

    Nana Naisbitt

    Founder of Chalkboard

    When Dr. Marlin Rice, back in a 2015 interview, asked Erwin how he would like others to remember him, his answer was simple – by what his students do. The influence a mentor has on their students and them on theirs, he described, is an unbroken chain that keeps connecting generations of thinkers. Erwin told Rice, “There’s this chain all the way from the great old-timers down through George [Ball – his Ph.D. mentor] and his students and what I’d like to do is to keep that chain going.”

    Indeed, Erwin’s brilliance, passion, and dedication for science extended those chains far beyond his students and colleagues, to countless others across space, like me. As the value of his research will certainly endure, those chains will also extend across time. Erwin was undoubtedly one of the rare ones among us whose influence has had, and will continue to have, an extraordinary reach.

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    Starving for data and more: what rangers and scientists stand to learn from one another in South Africa

    Starving for data and more: what rangers and scientists stand to learn from one another in South Africa

    Starving for data and more: what rangers and scientists stand to learn from one another in South Africa

    A one-year pilot biomonitoring program in Kruger National Park, South Africa – the Kruger Malaise Program – reignites rangers' energy about biodiversity conservation.

    Silhouette of a giraffe in Kruger National Park, South Africa

    PHOTO CREDIT: Michelle D’Souza

    Insect biodiversity is understudied and often underappreciated. As evidence for large-scale insect declines emerge, there is an increasing need to address the extreme lack of data on the general ecology and population dynamics of most insect groups. Charismatic species, such as the iconic monarch butterflies (Danaus plexippus) of the Americas, are one of the few exceptions.

    Closely related to the migratory Danaus plexippus, the non-migratory monarch species – Danaus chrysippus – is found in the warm climate of the African continent.
    PHOTO CREDIT: Johandre van Rooyen

    The caterpillars of the Emperor moth (Gonimbrasia belina) are just as iconic and societally relevant on the African continent. Locally referred to as ‘mopane worms’ after the mopane trees upon which they primarily feed, these insects have been a vital source of protein for generations. A mopane caterpillar contains on average 50 per cent protein1, a higher percentage than the average steak.

    In recent years, mopane caterpillars have also provided an important source of income for many rural communities. It has been estimated that 9.5 billion caterpillars are harvested annually in Southern Africa’s 20,000 km2 of mopane forest. The ability to predict mopane caterpillar outbreaks in space and time becomes increasingly valuable, particularly for rural communities living along the borders of national parks, who rely heavily on natural resources to supplement their livelihood.

    Mopane worm harvest in Kruger National Park, South Africa.
    PHOTO CREDIT: Louise Swemmer

    Local community members harvesting mopane worms in the Kruger.
    PHOTO CREDIT: Louise Swemmer

    Since 2010, permit-based harvesting projects have taken place in some South African National parks to share benefits and build positive relationships between the parks and their neighbouring communities. With the declining occurrence of mopane caterpillars outside of protected areas due to habitat change and over-harvesting, and the overall erratic nature of recent outbreaks, neighbouring communities risk losing an important source of food and income.

    A better understanding of insect dynamics has the potential to inform the sustainable harvest of natural resources such as the mopane caterpillar, but it also tells us a lot more.

    A pilot insect biomonitoring program in Kruger National Park, South Africa – the Kruger Malaise Program – is already demonstrating implications for natural resource harvesting, as well as agricultural pest and disease management. Perhaps even more significant, it has reignited energy in park rangers about biodiversity conservation.

    One of 26 Malaise traps sampling insects in Kruger National Park with the Kruger Malaise Program.
    PHOTO CREDIT: Ryan Rattray

    The Kruger Malaise Program (KMP), a year-long monitoring effort, was undertaken in Kruger Park from May 2018 to June 2019. With the main goal of understanding insect diversity and seasonal variation, the program deployed 26 Malaise traps that sampled the flying insect community in all 22 sections of the park. Traps were set up within each section ranger’s property, and rangers were tasked with organizing and maintaining weekly sample collections. The samples were then retrieved in four large batches over the year by staff from the African Centre for DNA Barcoding (ACDB) in Johannesburg, South Africa, where they were packaged and shipped to the Centre for Biodiversity Genomics (CBG) in Guelph, Ontario, Canada for DNA barcode analysis. This program was only possible due to the collaborative efforts of park rangers and staff, researchers at the Savanna & Arid Research Unit in Skukuza, Kruger, and scientists at the ACDB and CBG.

    The African Centre for DNA Barcoding (ACDB) team after collecting the last Malaise trap at the end of the KMP in June 2019: Zandisile Shongwe, Nolo Sello, Michelle van der Bank (ACDB Director), Ross Stewart, Jonathan Davies (top left to right), Johandre van Rooyen (bottom).
    PHOTO CREDIT: Nolo Sello

    With sampling now complete, analysis has begun in earnest. So far, more than 260,000 specimens have been processed, and 170,000 have been sequenced.  Preliminary results have delivered barcode coverage for 9,000 species including various agricultural pests (e.g., the olive fruit fly (Bactrocera oleae), and the rusty plum aphid (Hysteroneura setariae)) as well as several vector species known to transmit the bluetongue and African horse sickness viruses (e.g., Culicoides imicola) and West Nile Virus (Culex perexiguus). When compared against the DNA barcode database (BOLD Systems) of more than 600,000 species, almost half of the insect diversity uncovered by the program so far is only found in Kruger. Based on species accumulation rates, it is likely that 25,000 species will be recorded in the park. This number represents more than half of the species previously reported from South Africa2, and quarter of those described in sub-Saharan Africa3.

    Selection of specimens collected from the Kruger Malaise Program.
    PHOTO CREDIT: CBG Imaging Lab

    The Kruger Malaise Program reveals just how quickly DNA barcoding can provide in-depth and broad-scale information for regions where past research has largely been focused on particular taxonomic groups.  While one of the only comprehensive field guides for insects in South Africa contains 1,200 species – those that are ‘abundant, widespread, conspicuous, large or unusual’ – the Kruger Malaise program has largely uncovered the rare, small, inconspicuous, yet ecologically important, species.

    In 2013, SANParks developed a biodiversity monitoring strategy but its activation has been very mixed across the 19 parks. Some began their monitoring efforts by focusing on rare species, while others used key indicator groups. But there have been no standardized techniques implemented across all parks, and there has been little monitoring of insects at a large scale, mainly because of the lack of taxonomic expertise. A program involving DNA technology makes large-scale biomonitoring of these national parks possible.

    The KMP has been a huge success with the next steps set to fine tune logistics before its expansion to other parks and, ideally, to identify specific sites in Kruger for ongoing monitoring. The program also provided a test bed for TRACE (Tracking the Response of Arthropod Communities to Changing Environments), a major research theme within the 7-year, $180 million BIOSCAN program. Its success has demonstrated the feasibility of extending this work in other national parks within South Africa and on a global scale. In doing so, BIOSCAN will lay the foundation for a DNA-based global biodiversity observation system, similar to the monitoring systems that have been recording weather patterns since the 1800s. BIOSCAN has a grand vision, one that is necessary if we are to truly identify, understand, and manage the global decline in insects.

    The park rangers and staff who managed the Malaise traps in Kruger National Park.
    PHOTO CREDIT: Michelle D’Souza

    But if you ask the people working in Kruger, the KMP was more than a biodiversity monitoring program. Most rangers start out as nature conservation and zoology students, but anti-poaching efforts are so time consuming that their roles have gone from biodiversity managers to single-species protectors. The KMP has not only sparked interest and reignited energy in the park rangers about their conservation work, it has engaged and valued the observational and experiential data that rangers have to offer, such as stories and strategies related to the mopane caterpillars.

    In this way, the KMP has made a very big impact – and that is the true beauty of the program – its ability to spur interest in insect life, and the patterns and processes that define our world.

    Please feel free to contact Michelle D’Souza, the KMP project manager, if you have any questions about the program: mdsouza@uoguelph.ca

    References:

    1. Glew RH, Jackson D, Sena L, VanderJagt DJ, Pastuszyn A and Millson M (1999) Gonimbrasia belina (Lepidoptera: Saturniidae): a Nutritional Food Source Rich in Protein, Fatty Acids, and Minerals. American Entomologist 45(4): 250–253

    2. Scholtz CH and Chown SL (1995) Insects in southern Africa: how many species are there? South African Journal of Science 91:124–126

    3. Miller SE and Rogo LM (2002) Challenges and opportunities in understanding and utilisation of African insect diversity. Cimbebasia 17:197–218

    Written by

    Michelle L. D'Souza

    Michelle L. D'Souza

    Centre for Biodiversity Genomics, Guelph, ON, Canada

    Danny Govender

    Danny Govender

    General Manager: Savanna and Arid Research Unit, South Africa

    June 12, 2019
    doi: 10.21083/ibol.v9i1.5471

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