Changes to the composition of scale insect species (Coccomorpha: Eriococcidae) on New Zealand mānuka (Leptospermum scoparium; Myrtaceae) in the last seventy years

ABSTRACT

The perception of Leptospermum scoparium (mānuka) in New Zealand has changed from a weed to a valued shrub over the last half century due to the economic benefits of mānuka honey. The scale insect Acanthococcus orariensis (Hoy) (Hemiptera: Eriococcidae), an accidental control agent of L. scoparium that caused the mānuka blight mass dieback in the 1940s, initially was common, but declined once the entomogenous fungus Angatia thwaitesii (Petch) Arx (Fungi: Myriangiaceae) appeared. Subsequently, Acanthococcus campbelli (Hoy) and Acanthococcus leptospermi (Maskell) appear to have replaced Ac. orariensis in the last few decades, but there is limited knowledge on their current distribution. The distribution of Acanthococcus species on L. scoparium was determined at 28 sites throughout New Zealand. The most widespread species was Ac. leptospermi, which was found at 23 sites, whereas Ac. campbelli was found at 13 sites, and Ac. orariensis at just two sites. It appears that Ac. leptospermi is now the most common Acanthococcus species on New Zealand Leptospermum, and the blight caused by Ac. orariensis has not returned.

KEYWORDS:

• Acanthococcus campbelli
• Acanthococcus leptospermi
• Acanthococcus orariensis
• distribution survey
• Eriococcidae
• mānuka blight
• mānuka honey
• sooty mould

Introduction

New Zealand harbours approximately 370 scale insect species (Hemiptera: Coccomorpha) (García Morales et al. 2016), with approximately 270 species native to New Zealand (Henderson 2009). They are classified into ten families, with the Eriococcidae, commonly known as felt scale insects, being the largest family (ca 100 species) in New Zealand (Hoy 1954, 1958, 1959, 1962; Hodgson 1994; Hodgson and Henderson 1996; Henderson 2006, 2007a, 2007b; Henderson et al. 2010). This family is diverse in the Southern Hemisphere and is usually hosted by species of the family Myrtaceae (Gullan et al. 2004). The family Eriococcidae is characterised by a high degree of generic endemism in New Zealand (66%) (Henderson 2009). However, despite this high level of endemism, there are also species such as Acanthococcus orariensis Hoy (formerly in Eriococcus Targioni Tozzetti; Miller and Gimpel (1996)) that arrived accidentally from Australia (Hoy 1954). This eriococcid species is hosted by Leptospermum scoparium J.R. Forst et G. Forst (mānuka; Myrtaceae) (Hoy 1954, 1961), which is indigenous to New Zealand and Australia (Thompson 1989).

Leptospermum scoparium has had a controversial place in New Zealand ecology (Essien et al. 2019). For farmers it reduced the agricultural land value by overtopping pasture (Gardiner 1953), but for conservation, this species played a significant role as a nurse species for other native trees as well as reducing erosion risk in hill country (Hoy 1949; Sewell 1949; Campbell 1953). An opportunity for controlling L. scoparium appeared in 1937 in Orari Gorge (Canterbury), where Ac. orariensis was first found and initially it remained restricted to that part of Canterbury, before it was deliberately spread onto North and South Island farms by landowners in the 1950s in an attempt to control the plant (Hoy 1954, 1961). Further investigations revealed the species to be native to Australia where it occurs on Leptospermum species, including L. scoparium (Hoy 1959), and had presumably arrived into New Zealand unaided prior to 1937 (van Epenhuijsen et al. 2000). In New Zealand, Ac. orariensis is associated with the sooty mould Capnodium walteri Sacc. (Fungi: Capnodiaceae), which grows prolifically on the honeydew produced by Ac. orariensis (Mulcock 1954). Both agents were together recognised as the cause of mānuka blight in New Zealand that had caused widespread localised death of many mānuka stands throughout the country at the time following its deliberate spread (Hoy 1961).

The efficiency of Ac. orariensis as control agent for L. scoparium was suggested to be due to the release from its natural enemies once in New Zealand and the density of the infestations on mānuka (Hoy 1961). The subsequent recovery of L. scoparium in 1954 in Te Reinga (Gisborne) prompted investigation as to why and led to the discovery there in 1957 of the host-specific entomogenous fungus Angatia (formerly Myriangium) thwaitesii (Petch) Arx (Fungi: Myriangiaceae) parasitising Ac. orariensis (Hoy 1961).

The prevalence of Ac. orariensis appeared to decrease on L. scoparium with the colonisation of An. thwaitesii (Hoy 1961). This coincided with the increase of a second Australian scale insect Acanthococcus leptospermi (Maskell), which had been first reported in 1949 (Hoy 1961; van Epenhuijsen et al. 2000). This species does not appear to be affected by An. thwaitesii (van Epenhuijsen et al. 2000), which may help to explain its increase in abundance in New Zealand. A third species of Australian Acanthococcus, Ac. campbelli (Hoy), was recently reported on L. scoparium in New Zealand (Gardner-Gee and Beggs 2009; Henderson et al. 2010). Whereas Ac. leptospermi seems to be relatively harmless to L. scoparium (van Epenhuijsen et al. 2000), the damage caused by Ac. campbelli was suggested to be more significant than that done by Ac. orariensis in an Australian survey (Hoy 1959). Hoy (1961) considered Ac. campbelli as a potential future control agent against L. scoparium in New Zealand, so its recent discovery in New Zealand is significant.

The distribution of Ac. leptospermi has not been updated since 1959 (Hoy 1961) and is unknown for Ac. campbelli. Given Hoy’s prognosis on the damage likely from Ac. campbelli, and the current interest in mānuka farming due to the antibacterial and antioxidant properties of its honey (Allen et al. 1991; Speer et al. 2015; McPherson 2016; Ministry for Primary Industries 2016) there is a need for further research determining the diversity and distribution of eriococcid species on L. scoparium in New Zealand. In this study, we undertook a survey of eriococcid species present on L. scoparium throughout New Zealand to update and illustrate the distribution of eriococcids in 28 locations throughout the country.

Material and methods

Sites with L. scoparium (n = 28) were visited between March 2015 and January 2017 (Table 1). The sites all contained accessible stands of L. scoparium and were chosen haphazardly across a wide area throughout New Zealand, but the survey did not cover the entire range of the species. Stem samples infested with sooty mould and scale insects (Figure 1) were collected and placed in zip-lock plastic bags until further examination. In the laboratory, stems were assessed under a dissecting microscope. Fine forceps were used to uncover the waxy sacs of immature males and adult females present on stems; specimens at different life stages were preserved in 70% ethanol. Adult females were slide-mounted for identification following the protocol of Gullan (1984) and specimens identified using taxonomic keys (Hoy 1959; Hoy 1962; Morales 1991; Henderson 2011). Specimen slides provided by the New Zealand Arthropod Collection (NZAC) were examined to corroborate identification of different species made from the keys.

Figure 1. Sooty mould and scale insects on Leptospermum scoparium. A, Stand of L. scoparium infested with sooty mould at Lake Wilkie (Southland, South Island). B, Crawlers (first-instar nymphs) emerging from adult female sacs and nymphs settled on a fork of L. scoparium. C, Typical black ‘mantle’ that coats leaves and stems on L. scoparium due to sooty mould and scale insect infestation. D, Plant of L. scoparium infested with sooty mould. E, Dead adult female enclosed in felted cotton sac.

Table 1. Locations sampled between March 2015 and January 2017; includes location number assigned in Figure 2, NZ official place names, number of slide-mounted specimens per location, and latitude and longitude.

Location number	NZ official place names	Number of specimens that were mounted	Latitude	Longitude
1	Palmerston North City	26	40°23.24′S	175°36.66′E
2	Lake Rotorua/Te Rotorua nui ā Kahumatamomoe	5	38°08.15′S	176°15.70′E
3	Rotorua Domain Recreation Reserve	4	38°08.01′S	176°14.68′E
4	Rainbow mountain	3	38°18.93′S	176°23.24′E
5	Whangākea/Pandora	2	34°27.14′S	172°46.68′E
6	Waiheke Island Scenic Reserve	3	36°49.29′S	175°04.82′E
7	Coromandel Forest Park	4	37°02.66′S	175°42.44′E
8	Stony Bay Creek	4	36°30.35′S	175°25.15′E
9	Ruakokoputuna River	7	41°18.51′S	175°28.31′E
10	Motutere/Castle Rock	7	36°47.95′S	175°33.98′E
11	Ruatiti Scenic Reserve	12	39°17.91′S	175°12.30′E
12	Rangitatau Scenic Reserve	14	39°45.89′S	174°52.75′E
13	Tutira Domain Recreation Reserve	14	39°13.34′S	176°55.12′E
14	Ruahine Forest Park	5	39°52.55′S	175°58.58′E
15	Pahaoa Scientific Reserve	5	41°21.48′S	175°45.05′E
16	Pourangahau/Mount Roberts	7	41°47.78′S	172°49.65′E
17	Isolation Creek	5	41°53.91′S	174°01.85′E
18	Lewis Pass Road Scenic Reserve	9	42°31.02′S	172°23.21′E
19	Jollies Pass Scenic Reserve	8	42°28.30′S	172°52.98′E
20	Franz Josef/Waiau	6	43°15.55′S	170°13.55′E
21	Anatoki River	3	40°51.19′S	172°44.13′E
22	Totaranui	2	40°49.36′S	173°00.18′E
23	Horseshoe Point 1	6	46°52.69′S	168°08.89′E
24	Peterson Hill	6	46°54.09′S	168°08.02′E
25	Horseshoe Point 2	9	46°52.71′S	168°08.70′E
26	North Arm Point	4	46°52.58′S	168°01.64′E
27	Mill Creek	5	46°53.46′S	168°06.58′E
28	United Creek	0	41°09.16′S	172°40.34′E

Results

During the survey, 185 adult female specimens of Acanthococcus were slide-mounted and identified. Only three eriococcid species were found: Acanthococcus campbelli, Ac. leptospermi and Ac. orariensis. Acanthococcus leptospermi was the most widespread being present at all but five locations (Lewis Pass Road, Peterson Hill Road, Ruakokoputuna, Waima Road, and United Creek) (Figure 2). Acanthococcus campbelli was the second most abundant scale species and was found in the southern half of North Island, a third of the South Island and on Stewart Island. Acanthococcus campbelli was found at two sites (Lewis Pass Road and Waima Road) where Ac. leptospermi was not found. Acanthococcus orariensis was found at only two sites, both in South Island (West Coast and Totaranui). United Creek (Nelson) was the only site where no Acanthococcus species were found. During the survey, no plant or branch death was apparent from the infestations, despite scale insects often being frequent.

Figure 2. The distribution of Acanthococcus species present on samples of L. scoparium collected between March 2015 and January 2017. Numbers refer to locations outlined in Table1; 1–15: North Island locations, 16–22: South Island locations, 23–27: Stewart Island locations.

In addition to Acanthococcus species, 36 specimens from other scale insect families were found. Of these, 25 specimens were identified as belonging to the Coelostomidiidae, nine as Pseudococcidae and two as Diaspididae.

Slide specimens of all scale insect have been deposited in Te Papa Tongarewa Museum of New Zealand, Wellington, New Zealand (NMNZ).

Discussion

This study shows that Ac. campbelli and Ac. leptospermi are widespread throughout New Zealand. In contrast, the previously widespread Ac. orariensis was found at only two of 28 sites. These results suggest that the three Acanthococcus species occurred on L. scoparium in New Zealand in distinct stages of replacement. The early stage was characterised by the incursion of Ac. orariensis, which fatally damaged many of its host plants in the 1940s and 1950s (Hoy 1961). Following the control of Ac. orariensis by An. thwaitesii, a transitional stage resulted in the replacement of Ac. orariensis by Ac. leptospermi, which became the most abundant species in the 1990s (van Epenhuijsen et al. 2000). The current stage appears to be characterised by the arrival and spread of Ac. campbelli, which, together with Ac. leptospermi, is now widely distributed around New Zealand (Figure 2). Acanthococcus campbelli was reported first on L. scoparium in the Auckland region in 2009 (Gardner-Gee and Beggs 2009; Henderson et al. 2010), but its wider distribution in New Zealand was unknown until the present study.

The spread of Ac. campbelli and Ac. leptospermi, and the disappearance of Ac. orariensis could be due to the apparent immunity of the former two species to the entomogenous fungus An. thwaitesii, which attacks Ac. orariensis (Hoy 1961) and is thought to have significantly reduced the latter’s population. This replacement was predicted by Hoy (1961), who suggested Ac. leptospermi would become the dominant species in the future. Thought not apparently yet present in New Zealand, Hoy also suggested Ac. campbelli would be a potential future control agent of L. scoparium and other Leptospermum species (Hoy 1959) and he suggested research on the interaction between Ac. campbelli and An. thwaitesii be conducted (Hoy 1961), but this was never carried out. The present study shows that Ac. campbelli is now widespread in New Zealand, but its potential susceptibility to An. thwaitesii is still unknown.

Acanthococcus orariensis is also preyed on in New Zealand by the Australian ladybird Rhyzobius ventralis Erichson (Coccinellidae) (Zondag 1977), although R. ventralis is mainly associated with the gum tree scale Ac. coriaceus (Miller & Gimpel) (Kirk 1908). So, it might be that, along with An. thwaitesii, the absence of R. ventralis facilitates the establishment of new colonies of Ac. campbelli and Ac. leptospermi, as this predator has not been previously recorded on either species.

There are likely to be other natural enemies of these scale insects in Australia. There have been no recorded scale outbreaks on Leptospermum in Australia and scales are apparently kept are low numbers due to the large number of predators and parasitoids species (Gough 1975). However, as Ac. campbelli and Ac. leptospermi are introduced in New Zealand, the lack of predators and parasitoids, may explain their dispersion and success on L. scoparium in New Zealand.

Acanthococcus campbelli and Ac. leptospermi are now widespread on L. scoparium in New Zealand, although there are still regions where they have not been recorded. This suggests a need to continue survey work to help identify the ongoing spread of Ac. campbelli and its potential influence on the productivity of L. scoparium. Research to evaluate the influence of Ac. campbelli on L. scoparium, and the susceptibility of Ac. campbelli to An. thwaitesii is important and would be of interest to both ecologists and mānuka honey producers.

Acknowledgements

We would like to acknowledge Mānuka Farming NZ and the Primary Growth Partnership (New Zealand Ministry for Primary Industries, Manatū Ahu Matua) awarded to Manuka Research Partnership (NZ) Limited, and Comvita Limited for funding and advice. The authors would like also to thank Massey University for the Doctoral Research Dissemination Grant, landowners for permission to sample and the New Zealand Arthropod Collection for the loan of material. The suggestions and corrections made by the two anonymous reviewers are also appreciated.

Disclosure statement

No potential conflict of interest was reported by the authors.

ORCID

Julia Bohórquez http://orcid.org/0000-0002-0871-3561

Alastair W. Robertson http://orcid.org/0000-0001-6894-2158

Additional information

Funding

Funding received from a Primary Growth Partnership grant (New Zealand Ministry for Primary Industries), “High-performance mānuka plantations”, awarded to Manuka Research Partnership (NZ) limited, and from a Massey University dissemination grant to JB.