NA Martin 23

Insect-host association: how Plant-SyNZtm provides information on the quality of supporting evidence

Nicholas A. Martin

Research Associate, Landcare Research, Private Bag 92170, Auckland 11072. [email protected]

Very early in the formation of the Plant-SyNZtm database I realised that it was important to show the quality of evidence supporting the association of a herbivore species with a host plant species. The literature varies in its approach. I will take as an example Spencer (1976) who describes Agromyzidae of New Zealand (Insecta: Diptera) and I will focus on the genus Phytoliriomyza (Diptera: Agromyzidae). I have chosen this genus because the association of two Phytoliriomyza species with silver , Cyathea dealbata, were highlighted in a recent paper (Thorpe 2021).

The Plant-SyNZtm database has a table for herbivore/plant associations and forms for recording and showing information. The key form (Figure 1) shows the name of the herbivore, the host plant, and the reference in which details of the association were published. It also summarises the evidence for the association and gives this a reliability score from 1-10, where for a leaf miner, for example, 10 is for rearing an adult from a larva and/or pupa found in the host plant. The form also shows the name of the assessor and the date of assessment.

Three species in the genus Phytoliriomyza, (P. cyathea, P. flavopleura and P. tearohenis) have genitalia that show they belong to a group of species whose larvae are fern feeders (Spencer 1976). Spencer (1976) reports that adults of P. cyathea were found on Cyathea dealbata and C. smithii at three locations in December and early January and that larvae in mines were present in December and early January (see Figs 2-5 for examples). 24 The Wētā 55:23-33

However, no adults were found on where larvae were feeding and because the larvae leave the mines to pupate no adults have been reared from larvae in mines. Therefore, the association between P. cyathea and the two Cyathea species was given a score of 8 (Table 1). I have also found mines in a third species of Cyathea and because no adults were found or reared I gave it a score of 7 (Table 1).

Figure 1. Plant-SyNZ form showing the evidence for the association between a herbivore and its host plant.

Spencer (1976) only found one male of P. tearohenis, and this was on C. dealbata. He comments that “It can never be assumed that the presence of a fly on a particular plant indicates that this is its host but in this case there seems a strong possibility that Alsophila [Cyathea] is the host.” In the Plant- SyNZ database I took the view that a single adult male fly sitting on a plant was not adequate evidence of a host association, whereas a single adult female ovipositing would provide strong evidence (although females cannot always be identified to species). NA Martin 25

When I found mines in C. cunninghamii, they were similar to those found on the other two species of Cyathea, that are made by Agromyzidae larvae, so I gave the association a score of 7.

The third species with fern feeder type genitalia is Phytoliriomyza flavopleura. It has host plants in four fern genera (Table 2). The fly pupates within the frond making it easier to rear adults. For this fly species, there is good evidence for eight host plants in three families, moderate evidence for a ninth species, but a tenth potential host species received a score of only 1! The comment about the behaviour of the larvae in Blechnum fluviatile frond refers to them moving from one pinna to another by burrowing through the stalk of the frond. Now that I have reread Spencer (1976) I realise that P. flavopleura larvae do this in other .

The internet version of the Plant-SyNZ database gives users the option of having a list of host plants of a herbivore or having a list with reasons. Both lists contain the ‘Reliability score’ (Table 3). The web site was last updated in 2015. As well as showing the plants associated with a species of herbivore, the database can show the species of herbivores associated with a plant species (Table 4). In the non-internet database, I treat the evidence supporting the relationship between a predator and its prey and a parasitoid and its host in a similar way to herbivores and plants.

The best solution to the issues raised in an earlier article by Stephen Thorpe (2021), is to rear adults from the agromyzid fly larvae found mining Cyathea fern fronds. Because Thorpe (2021) believes there could be two Phytoliriomyza exploiting Cyathea, adults should be reared from all three species of Cyathea that have so far been found with mines, and, ideally, from several geographic locations. Larvae have been found in frond mines in November, December, and January, but leave the mine to pupate (Figure 6). The difficulty to the rearing process is that the pupae must be kept alive until the adults emerge in late spring. 26 The Wētā 55:23-33

Figure 2. The upper surface of a frond of a Soft tree fern, Cyathea smithii with leaf mines caused by larvae presumed to be Phytoliriomya. cyathea (Agromyzidae).

Figure 3. Larva of Phytoliriomya. cyathea (Agromyzidae) in its mine in silver fern, Cyathea dealbata. Note the black mandibles being used to rasp frond tissue. NA Martin 27

In the meantime, we are left with the possible discovery of a pair of P. tearohensis sitting on an unknown plant, which, if correct, would represent only the 2nd and 3rd specimens of this species to be collected (Thorpe 2021). In 2001 when I assessed the evidence for the association of P. cyatheae with ferns, C. dealbata and C. smithii, I gave the association a score of 8, hoping that one day I would rear adults and resolve the issue. This example illustrates the advantage of the Plant-SyNZ approach to plant-insect associations: a name can be tentatively assigned to un-reared larvae, and this information gathered with other evidence before making statements regarding a definitive association.

Acknowledgements

The author wishes to thank Landcare Research for developing and hosting the Plant-SyNZ web site.

References

Martin NA. 2017. Spleenwort fern leafminer - Phytoliriomyza flavopleura. Interesting Insects and other Invertebrates. New Zealand Arthropod Factsheet Series Number 80. nzacfactsheets.landcareresearch.co.nz/ Index.html. Spencer KA. 1976. The Agromyzidae of New Zealand (Insecta: Diptera). Journal of the Royal Society of New Zealand. 6 (2): 153-211. Thorpe S. 2021. Agromyzid leaf miners on silver fern: not so simple? The Wētā 55:16-17. Watt MN. 1923. The leaf-mining insects of New Zealand: part III-Species belonging to the genera Agromyza (Fallen) and Phytomyza (Fallen) (Diptera). Transactions and Proceedings of the New Zealand Institute. 54: 465-489. 28 The Wētā 55:23-33

Table 1. Phytoliriomyza cyathea Spencer 1976 and its probable host plants recoded in the Plant-SyNZ database.

Cyathea sp. Reliability Assessor, Reasons for association and score Date of score assessment

dealbata 8 adults found on host plant, MartinNA, 28 genitalia of type associated with Sep 01 fern feeders, agromyzid mines found in host plant (Spencer 1976, pages196-197)

smithii 8 adults found on host plant, MartinNA, 28 genitalia of type associated with Sep 01 fern feeders, agromyzid mines found in host plant (Spencer 1976, pages196-197)

cunninghamii 7 leaf mines on host plant similar to MartinNA, 28 those on other Cyathea species. Sep 01 (NA Martin in 2001)

Figure 4. larva of Phytoliriomya. cyathea (Agromyzidae) out of its mine in silver fern. Note the black mandibles being used to rasp frond tissue. NA Martin 29

Table 2. Host associations of Phytoliriomyza flavopleura Spencer 1976 recorded in Plant-SyNZ database.

Host plant Reliability Reasons for association and score Date of score assessment

Asplenium 10 Reared from host plant (N A Martin 2002) 15 Oct 02 appendiculatum

Asplenium 10 Reared from host plant (NA Martin 2001) 28 Sep 01 bulbiferum

Asplenium 9 Recorded as host plant, but not clear if flies were 28 Sep 01 flaccidum reared from host (Watt 1923, page 481), mines with larvae found by NA Martin

Asplenium 10 Reared from host plant (Watt 1923, p 482) plant 28 Sep 01 oblongifolium name given as A. lucidum; and reared by NA Martin

Asplenium 10 Agromyzid mines found in host plant (Spencer 02-Mar-18 polyodon 1976), plant name given as Asplenium falcatum

Blechnum 1 Watt (1923) records this as a host plant, but 28 Sep 01 filiforme Spencer (1976) argues that it was mistaken identity for Phymatodes scandens (= Microsorum scandens); no leaf mines have been found in B. filiforme by J Dugdale or NA Martin

Blechnum 10 Reared from host plant (NA Martin 2002), but 28 Sep 01 fluviatile adult fly has dark sternal triangle and different behaviour in leaves

Microsorum 10 Listed as host plant (Harrison 1959, p 320), plant 01-Apr-05 pustulatum name given as Polypodium diversifolium and fly as Phytobia flavopleura; but not clear if reared (Polypodiaceae) from host (reared from host plant by NA Martin 2004)

Microsorum 10 reared from host plant (NA Martin 2000) 28 Sep 01 scandens

Notogrammitis 7 Recorded as host plant (Watt 1923) plant name 28 Sep 01 billardierei given as Polypodium australis, but not certain if reared from host plant 30 The Wētā 55:23-33

Table 3. Host associations of Phytoliriomyza cyathea Spencer 1976 presented in the Landcare Research web site for Plant-SyNZ, https://plant- synz.landcareresearch.co.nz/SearchForm.aspx. There are two options, a simple report and a report with reasons.

Report

7 Cyathea cunninghamii Hook.f. in Hook., (Cyathea tree fern family), , Polypodiopsida, Pteridophyta. Biostatus: Indigenous, Wild, New Zealand

8 Cyathea dealbata (G.Forst.) Sw., Cyatheaceae (Cyathea tree fern family), Cyatheales, Polypodiopsida, Pteridophyta. Biostatus: Endemic, Wild, New Zealand

8 Cyathea dealbata (G.Forst.) Sw., Cyatheaceae (Cyathea tree fern family), Cyatheales, Polypodiopsida, Pteridophyta. Biostatus: Endemic, Wild, New Zealand

Report with reasons

7 Cyathea cunninghamii Hook.f. in Hook., Cyatheaceae (Cyathea tree fern family), Cyatheales, Polypodiopsida, Pteridophyta Biostatus: Indigenous, Wild, New Zealand Reasons for score: leaf mines on host plant similar to those on other Cyathea species. (NA Martin in 2001) Scored by: N.A. Martin

8 Cyathea dealbata (G.Forst.) Sw., Cyatheaceae (Cyathea tree fern family), Cyatheales, Polypodiopsida, Pteridophyta Biostatus: Endemic, Wild, New Zealand Reasons for score: adults found on host plant, genitalia of type associated with fern feeders, agromyzid mines found in host plant (Spencer 1976, pages196-197) Scored by: N.A. Martin

8 Cyathea smithii Hook.f., Cyatheaceae (Cyathea tree fern family), Cyatheales, Polypodiopsida, Pteridophyta Biostatus: Endemic, Wild, New Zealand Reasons for score: adults found on host plant, genitalia of type associated with fern feeders, agromyzid mines found in host plant (Spencer 1976, pages196-197) Scored by: N.A. Martin

NA Martin 31

Figure 5. A large larva of Phytoliriomya. cyathea (Agromyzidae) out of its mine in silver fern.

Figure 6. A pupa of Phytoliriomya. cyathea (Agromyzidae). 32 The Wētā 55:23-33

Table 4. Herbivores on the fern Asplenium polyodon (Aspleniaceae).

Score Herbivore Classification Biostatus Reasons for score

Agromyzid mines found Phytoliriomyza Diptera: in host plant (Spencer 10 flavopleura (Watt, endemic Agromyzidae 1976), plant name given 1923) as Asplenium falcatum

puparia found on fronds of host plant (NA Trialeurodes sp. Martin 2000) and Hemiptera: 9 'polyodon' of NA endemic differences in Aleyrodidae Martin 2010 appearance and behaviour observed in 2010

large aphid colony, including winged Idiopterus Hemiptera: specimens on fern frond 10 nephrelepidis adventive Aphididae found in June at Te Davis, 1909 Aroha Domain (NA Martin 2011)

Large colony of aphids on young expanding Micromyzella frond of plant in Orewa Hemiptera: 10 filicis (van der adventive reserve in May and at Aphididae Goot, 1917) Murphy's Bush, South Auckland in December (NA Martin 2016)

aphids in colony of another species fern, aphid on fern fronds in Rhopalosiphoninus forest reserve at Te Hemiptera: 5 latysiphon adventive Aroha in June 2011 Aphididae (Davidson, 1912) (NA Martin 2012, identified by B Foottit), no evidence of aphid breeding on fern NA Martin 33

mature scale on fern frond (NA Martin 2008, Saissetia coffeae Hemiptera: identified by RC 10 adventive (Walker, 1852) Coccidae Henderson 2008); Smiths bush, North Shore, Auckland

female scale found on Fusilaspis Hemiptera: host plant (NA Martin 10 phymatodidis endemic Diaspididae 2000, identified by RC (Maskell, 1880) Henderson)

Nymphs of several sizes on fronds on a plant on Siphanta acuta Hemiptera: 10 adventive Scenic Drive, Waitakere (Walker, 1851) Flatidae Ranges in April (NA Martin)

Felisacus Hemiptera: breeds on host plant 10 elegantulus native Miridae (Eyles & Schuh, 2003) (Reuter, 1904)

many small nymphs on an expanding frond of Scolypopa Hemiptera: plant in Waitakere 10 australis (Walker, adventive Ricaniidae Ranges during 1851) November (NA Martin 2010)

on underside of fern frond in webbing covered with fern Batrachedra sp. Lepidoptera: spores, no holes through 8 'Asplenium sori' endemic Batrachedridae frond to upper side (NA Dugdale 1988) Martin 2010), found on fern in Manurewa, Auckland in January