Kauri Dieback on Aotea

RICHARD WINKWORTH (Massey University)

In April 2021 the Department of Conservation announced that kauri dieback had been detected at two new sites on Aotea Great Barrier. These detections followed the largest testing programme yet undertaken on the island. The two new sites, one above the Kaitoke Swamp and one in the Awana catchment, bring the total of kauri dieback positive sites on Aotea Great Barrier to five. That this number remains in single digits despite it being nearly 50 years since the first detection is in stark contrast to trends in the Waitakere Ranges and elsewhere. What might these new detections mean?

Introduction

Kauri (Agathis australis, Araucariaceae) is New Zealand’s largest tree species growing to over 50 m tall and living for upwards of 1,000 years(1). Iconic to many New Zealanders and a culturally significant taonga to Māori, the long-term survival of kauri and the unique kauri forest ecosystem is threatened by an as yet incurable disease. Kauri dieback affects all age classes from seedlings to forest giants; symptoms of the disease include root rot, gummosis, crown thinning and, ultimately, tree death(2).

The late Peter Gadgil authored the first published account of kauri dieback(3). His study, at a site in the upper Kaitoke catchment, suggested that the causal agent was a member of the genus Phytophthora. This large group of fungus-like microorganisms contains many well-known plant pathogens. Yet, it was not until 2005-2006, when symptoms first appeared in the Waitakere Ranges and Waipoua Forest, that the significance of this earlier work became apparent. Although initially attributed to Phytophthora heveae(3), more recent analyses have identified the causal agent as Phytophthora agathidicida(4), a species that is closely related to P. heveae but distinctive enough to be formally recognised in its own right.

The kauri dieback pathogen, at the time referred to as “Phytophthora taxon Agathis” or PTA for short, was declared an unwanted organism in 2008. Since then, mana whenua, the Department of Conservation, Ministry for Primary Industries and local government have worked towards long-term management(2).

How do we test for kauri dieback?

Before we go any further it is important to point out that there is no test for kauri dieback. Kauri dieback is the disease, the collection of physical symptoms exhibited by an infected tree. Kauri dieback positive sites are identified on the basis of the appearance of symptoms. When we test, it is for P. agathidicida, the organism believed to be responsible for the disease. This distinction between disease and pathogen is an important one when it comes to understanding the survey results.

Testing for P. agathidicida typically involves a soil bioassay(5). Although the approach is well established, the time and cost involved limits the volume of testing that it is possible to conduct. Effectively, widespread pathogen surveillance has not been possible and instead sampling has focused on kauri dieback positive sites. The goal of testing at these sites is to confirm pathogen presence.

During the most recent survey of Aotea Great Barrier, aerial photography was used to identify locations of interest(6)(Figure 1). In this case a standardised procedure is used to evaluate photographs of the forest canopy for sites displaying symptoms consistent with kauri dieback (e.g., crown thinning). Ground teams then visited these sites to confirm the presence of kauri, check for disease symptoms (e.g., gummosis), and collect samples for P. agathidicida testing. Samples are not usually taken directly from diseased trees but instead consist of a few hundred grams of soil collected from around one or more trees at a site of interest.

Once in the laboratory the soil samples are first air dried, then sprayed with water and moist incubated for two or three days. This process stimulates the production of motile zoospores by P. agathidicida. After moist incubation the samples are flooded with water and plant tissue “baits”, often with cedar needles or lupin sprouts added. The samples are then left for two or three days to allow the zoospores of P. agathidicida and potentially those of other species to colonise the baits. From this point fairly standard microbiological approaches are used to isolate and establish cultures of the organisms that colonised the baits. Identifying isolates of P. agathidicida from amongst those recovered for a given sample relies primarily on morphology. A trained eye has to assess each isolate, looking for the physical features characteristic of this species. As a final step in this process the identity of isolates may be confirmed using a genetic test.

Interpreting the results

The results of the recent Aotea Great Barrier survey are clear. At two sites there is evidence, beyond the initial aerial photography, of the disease (e.g., gummosis) and the pathogen (e.g., a culture identified as P. agathidicida) whereas at the remaining 36 sites neither the disease nor the pathogen was found(6). However, interpreting these results is somewhat less straightforward.

Typically, new observations of kauri dieback are presumed to reflect pathogen spread. This explanation follows from a recommendation that P. agathidicida be treated as recently introduced until there was evidence otherwise(7). It implies both that disease-free kauri stands are pathogen-free and that disease is an inevitable outcome of pathogen arrival. Although plausible, because we typically test for the pathogen only after disease symptoms have appeared, there is very little data available against which to test this idea. Indeed, we know so little about the distribution of P. agathidicida away from kauri dieback positive sites that this explanation should probably be treated with greater caution than it currently is. Is there an alternative?

The disease triangle(8) views disease expression as a function of the interactions between pathogen, host, and environmental conditions rather than as an inevitable outcome of pathogen presence. Put another way, it suggests that the presence of P. agathidicida is just one of several conditions that need to be met before the symptoms of kauri dieback appear. Therefore, the appearance of kauri dieback in previously disease-free sites need not be intimately tied to pathogen spread. Instead, P. agathidicida could already be widespread with changes in biotic or abiotic environments resulting in conditions conducive to the appearance of kauri dieback. Such an explanation is not inconceivable. Kauri’s own life history traits (e.g., even-aged stands(9), (10)) and extreme reductions in the extent of kauri forests over the last 175 years(11) likely make this species vulnerable to dieback. Layer on top of this climate change(12), the introduction of potentially co-acting pathogens(13) and site-specific differences in soil type, aspect, hydrology and the intensity of human activity. There would certainly seem to be the potential for the relationship between kauri and P. agathidicida to have been pushed from benign to one of host and pathogen.

There is evidence from overseas to support a more holistic view of plant disease. For example, both biotic (e.g., secondary fungal infections) and abiotic (e.g., extremes in rainfall due to climate change) factors have been shown to contribute to Phytophthora-linked decline of stands of European beech (Fagus sylvatica L.) in Austria(12). For kauri dieback the focus has been so fixed on recent introduction and ongoing spread that little work has examined alternatives. That said, patterns of genetic diversity in P. agathidicida are consistent with this species having a much longer history in New Zealand(14) and, although the volume of testing away from kauri dieback sites remains limited, there is evidence of P. agathidicida being present in disease-free kauri stands(15). In themselves these results may not be conclusive, but they do not sit easily with current dogma; clearly much more work is needed in this space. Can we afford to simply ignore the possibility of alternative explanations?

Barrier survey and a recently published hybrid bioassay(16) suggest that the former is likely to underestimate the extent of the pathogen. For example, two of six soil samples from diseased stands in the Waitakere Ranges tested positive for P. agathidicida using the soil bioassay, whereas the hybrid bioassay detected pathogen in five out of six(16) . What might these results mean for kauri on Aotea Great Barrier? Drawing strong conclusions from a single round of testing is never easy. Often confidence comes only when repeated testing provides consistent results. That said, it is encouraging that since the disease was first reported on the island nearly 50 years ago, only four additional kauri dieback positive sites have been identified. Why has the number of positive sites increased more slowly on Aotea Great Barrier compared to, for example, the Waitakere Ranges? Ultimately, we do not know. Certainly the impact of human activity on forest health is likely to be much higher in the Waitakere Ranges, but there may not be a single explanation for such differences. Potentially, several factors contribute in combinations that differ between sites. Understanding the distribution of P. agathidicida is critical to the management of kauri dieback. We have, by necessity, tended to focus on kauri dieback positive sites and as a result have only part of the picture we need. On Aotea Great Barrier, as in most other areas, we need to be testing more widely and more often in order to inform decision making. Indeed the hybrid bioassay, which is more sensitive, less expensive and has shorter turn around times that soil bioassay, is already beginning to take testing from confirmation of pathogen presence to widespread surveillance(16), (17).

Conclusions

Fighting kauri dieback is immensely challenging. Much of what we know about fighting plant pathogens comes from agricultural systems. There is not a step-by-step guide with all the answers; instead we are trying to understand both pathogen and disease while simultaneously attempting to manage them. We are making headway but it remains difficult to provide much in the way of certainty.

Aotea Great Barrier has a long association with kauri dieback and the sad reality is that this disease is likely to remain a threat, both on the island and elsewhere, for some time. We need to get used to the idea that addressing this problem is likely to require a long-term commitment. Ultimately, the future of the kauri forest depends on everybody doing what is best for kauri.

Acknowledgements:

Many thanks to Lisa Tolich and Yue Chin Chew (Auckland Council) for provision of information about the recent Aotea Great Barrier kauri dieback survey and Wildlands Consultants and Auckland Council for aerial photographs. Also John Ogden for comments on age and structure of forests.

References:

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2. Bradshaw, R.E. et al. 2020. Phytophthora agathidicida: research progress, cultural perspectives and knowledge gaps in the control and management of kauri dieback in New Zealand. Plant Pathology 69: 3-16.

3. Gadgil, P.D. 1974. Phytophthora heveae, a pathogen of kauri. New Zealand Journal of Forestry Science 4: 59- 63.

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6. https://www.doc.govt.nz/news/media-releases/2021-media-releases/kauri-dieback-testing-confirms-twonew-sites-on-aotea-island/

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9. Ogden, J., Steward, G.H. 1995. Community dynamics of the southern conifers. In: Enright, N.J. & Hill, R.S. (eds.) Ecology of the southern conifers. Melbourne: Melbourne University Press. pp. 81-119.

10. Mueller-Dombois, D. 1993. Biotic impoverishment and climate change: global causes of forest decline? In: Huettl, R.F. & Mueller-Dombois, D. (eds.) Forest decline in the Atlantic and Pacific regions. Berlin: SpringerVerlag. pp. 357-429.

11. Steward, G.A., Beveridge, A.E. 2010. A review of New Zealand kauri (Agathis australis (D.Don) Lindl.): its ecology, history, growth and potential for management for timber. New Zealand Journal of Forestry Science 40: 33-59.

12. Corcobado, T. et al. (2020) Decline of European Beech in Austria: involvement of Phytophthora spp. and contributing biotic and abiotic factors. Forests 11: 895.

13. Bregant, C. et al. (2020) Diversity and pathogenicity of Phytophthora species associated with declining alder trees in Italy and description of Phytophthora alpina sp. nov. Forests 11: 848.

14. Winkworth, R.C. et al. 2021. The mitogenome of Phytophthora agathidicida: evidence for a not so recent arrival of the "kauri killing" Phytophthora in New Zealand. PLoS One 16: e0250422.

15. Beachman, J. 2017. The introduction and spread of kauri dieback disease in New Zealand. MPI Technical Paper 2017/52. Available from: https://www.kauridieback.co.nz/media/1487/2017-52-theintroduction-and-spread-of-kauri-dieback-disease-innew-zealand_final.pdf

16. Winkworth R.C. et al. 2020. A LAMP at the end of the tunnel: a rapid, field deployable assay for the kauri dieback pathogen, Phytophthora agathidicida. PLoS ONE 15: e0224007.

17. Biosense Ltd. 2020. Kauri dieback disease surveillance of Watercare’s proposed replacement water treatment plant site at Waima Catchment. Available from: https://wslpwstoreprd.blob.core.windows.net/kentico-medialibraries-prod/watercarepublicweb/media/watercare-media-library/huia/_kauri_dieback_disease_surveillance_report_nov_2020.pdf