Journal of East African Natural History 103(1): 31–38 (2014)

OBSERVATIONS ON AN IRRUPTION EVENT OF THE MOTH ACHAEA CATOCALOIDES (LEPIDOPTERA: EREBIDAE) AT

KAKAMEGA FOREST, KENYA

Dino J. Martins

Turkana Basin Institute, Stony Brook University N507 Social & Behavioural Sciences, Stony Brook NY 11794, USA

Insect Committee of Nature Kenya National Museums of Kenya, Museum Hill, Nairobi

P O Box 44486, Nairobi GPO 00100 Kenya dino@turkanabasin.org

Scott E. Miller

National Museum of Natural History, Smithsonian Institution Washington, DC 20013-7012, USA

MillerS@si.edu

Marina Cords Department of Ecology, Evolution and Environmental Biology, Columbia University

1200 Amsterdam Avenue, New York 10027, USA mc51@columbia.edu

Margaret T. Hirschauer, C. Barret Goodale

Kakamega Monkey Project PO Box 2579, Kakamega, Kakamega, Kenya

mhirscha@gmail.com, CBGoodale@gmail.com

ABSTRACT The moth Achaea catocaloides Guenee (Lepidoptera: Erebidae, formerly Noctuidae) experiences periodic population irruptions in tropical Africa. Large numbers of adult moths were observed in the Kakamega Forest, Western Kenya in March 2012. Estimated densities of adult moths flying in surveyed forest areas were 6.8 individuals per square metre. Roosting moth density was estimated at 12.7 individuals per 50 cm long branch on two common forest tree species: Croton megalocarpus and Bridelia micrantha. Based on scaled-up data from transect counts we conservatively estimate that this irruption contained 800 million – 1.5 billion moths. The Achaea moths were common throughout the indigenous forest and were being preyed on by birds and monkeys. These population irruptions occur periodically in African forests, but the underlying causes and factors driving them remain undetermined. DNA barcodes of Achaea catocaloides, Achaea catella and Achaea lienardi are provided to facilitate identification of future irruption events. Keywords: irruption, caterpillar outbreak, defoliation by insects, DNA Barcoding, croton

32 D.J. Martins, S.E. Miller, M. Cords, M.T. Hirschauer & C.B. Goodale

INTRODUCTION Drastic changes in abundance and population dynamics of tropical Lepidoptera are an interesting phenomenon of seasonal wet-dry environments such as those typical of Eastern Africa (Larsen, 1991). Short generation times and opportunistic behaviour can help insects increase rapidly in numbers and produce observed ‘outbreaks’ when they swarm or migrate locally (Holland et al., 2006). The moth genus Achaea Hubner (Lepidoptera: Erebidae) is well-known for periodic irruptions in tropical Africa, and reports of this phenomenon come from several countries in East and West Africa. Achaea catocaloides Guenee is the species most commonly recorded in this phenomenon. An early record of an A. catocaloides irruption was made by Pitman (1931), at Entebbe in Uganda. This moth was also observed as part of a fruit piercing feeding guild in Sierra Leone (Hargreaves, 1936). This phenomenon was also reported as an annual invasion of Accra, Ghana (Leston, 1979). A ‘moth plague’ was observed in Ghana in 1969, 1972 and 1973 that involved A. catocaloides and the related species A. liernardi (Boisduval) (Grubb, 1980). Achaea catocaloides has also been reported undergoing population explosions in Nigeria, including feeding on cultivated crops (maize Zea mays L. and cassava Manihot esculenta L.) (Eluwa, 1977). A study of defoliation in cocoa (Theobroma cacao L.) plantations in Cameroon found that ants were able to limit the effects of this moth (Dejean et al., 1991). Achaea catocaloides was documented defoliating a rainforest tree (Paraberlinea bifoliolata Pellegr.) in Gabon where large number of caterpillars were observed feeding on the trees and leaving trees by means of silken threads to pupate in the leaf litter below (Maisels, 2004). In late 2008 and early 2009, a very large irruption of Achaea catocaloides occurred in Liberia and Guinea. The 2009 event was so large that a national emergency was declared in Liberia because of crop damage and contamination of water supplies, capturing considerable attention from international news media (CABI 2009; G. Goergen, pers. comm., 2009).

We describe some observations of an irruption event in the Kakamega Forest, Kenya. The Kakamega Forest is a relict tropical rainforest fragment situated in western Kenya (0°19’N 34°52’E; ~1580 m). It is the last large area remaining in Kenya of the Guinea-Congolian rainforest that was once connected to the rainforests of the Congo Basin and Central Africa. The main block of forest (23 777 ha in 2003) includes two nature reserves and a national reserve, and comprises mixed vegetation types including near-natural and secondary forest, bushland, grassland and agricultural land. Natural forest covers 50% of this area (Mitchell et al., 2009). We base our estimates of natural/indigenous forest on these data as ~11 000 ha. Annual rainfall averages 1915 mm. Rain falls seasonally, typically with two annual peaks and a pronounced dry season from December through February (Bennun & Njoroge, 1999; Mitchell et al., 2009).

We do not have comprehensive records of previous irruptions at Kakamega, but we know that one occurred in 2001, with moths emerging in late May. J.M. Wathihi, District Forest Officer, reported (pers. comm. to Miller, 2001) defoliation of Bischofia javanica Blume, Cupressus lusitanica Mill., and pines (Pinus sp.) in Kakamega forest, and provided voucher specimens to National Museums of Kenya and the Smithsonian Institution. These were confirmed as Achaea catocaloides.

Achaea is a diverse genus of global distribution. The African taxa were reviewed by Berio (1965), who enumerated 35 species. Until recently, Achaea was placed in the Noctuidae, subfamily Catocalinae. Based on molecular studies that led to the extensive reclassification of the former Noctuidae, Achaea is now placed in the Erebidae, subfamily Erebinae (Holloway & Miller 2003; Holloway 2011).

Here we report observations of an Achaea catocaloides irruption that occurred in the Kakamega Forest in western Kenya in March and April 2012. We include estimates of adult

Irruption event of Achaea catocaloides 33

A. catocaloides abundance, which have not been made previously. We also report on the predation of the adult moths by birds and mammals in the forest. MATERIALS AND METHODS Observations of the moth Achaea catocaloides were made in March and April 2012 in the Isecheno area of the Kakamega Forest. The peak of the adult moth irruption occurred from approximately 18 March to 3 April 2012. Detailed observations on abundance were made between 25 March 2012 and 1 April 2012. The presence of moths in large numbers was recorded at multiple sites in the forest during the observation period (figure 1).

Figure 1. Sites (indicated by closed circles) at Kakamega Forest where abundance of A. catocaloides was quantified between 25 March–3 April. (a) location where large numbers of eggs were observed on March 1, and moths peaked on 18–22 March. (b) Moth abundance peaks here 18–22 March. (c) Moth abundance peaks here 25 March–3 April. Note our assessment of ‘peak abundance’ is based on general observations that were conducted on a daily basis by field teams spending c. 9 hrs per day in the forest. Scale bar is 1 kilometre. Image courtesy of GoogleEarth. KFS = Kenya Forest Service HQ at Isecheno.

To estimate the local abundance of moths, we used two counting methods: short transects and beating of tree branches where moths were roosting. Transect estimates consisted of DJM walking slowly for 10 m and counting all moths flying across the transect area (a 1 m band) using a hand-held counter. This was repeated 5 times at each of five different sites (Rondo stream trail, junction to Lirhanda Hill, base of Lirhanda Hill, River Yala trail and along the main road through the forest; figure 1). Beating involved a gentle tap of a ca. 50 cm long branch of each of 2 common tree species in the forest (Bridelia micrantha (Hochst.) Baill. and Croton megalocarpus Hutch. (identified using Beentje [1994]) and counting the number of moths that flew out. Each branch was tapped only once so as to estimate the number of moths on that branch alone and not startle moths roosting in surrounding vegetation. This procedure was repeated 20 times for each plant species. We used transect and beating data to derive estimates of the abundance of A. catocaloides in the forest as a whole. Data were analysed with Microsoft Excel Version 14.2.4.

34 D.J. Martins, S.E. Miller, M. Cords, M.T. Hirschauer & C.B. Goodale

We observed predators feeding on the moths at the five counting sites while conducting

transects and walking through the forest. Blue monkeys also were observed by three of us (DJM, MTH & CBG) feeding on the moths at other nearby sites (figure 1) that are part of a long-term primate monitoring project in Kakamega Forest (Cords, 2012). Specimens were collected to confirm identification and these have been deposited as vouchers in the collections of the Smithsonian Institution and the National Museums of Kenya. Identity of specimens from the 2001 Kakamega irruption was confirmed by male genitalia (USNM slides 92502 and 125566, figure 2) using Berio (1965). COI (cytochrome oxidase I) sequences were generated at the Biodiversity Institute of Ontario, University of Guelph using standard DNA barcoding protocols (Miller, 2007; Craft et al. 2010).

Figure 2. Details of Achaea catocaloides. A. Representative adult specimen of A. catocaloides from West Africa. Scale bar is 10 mm. B. Main part of male genitalia from slide USNM 92502. C. Vesica from slide USNM 125566. D. Group of moths at light photographed at 7 am, 02 April 2012. E. Adult A. catocaloides at rest near a light at Kakamega Forest, Kenya. Scale bar is 10 mm.

Irruption event of Achaea catocaloides 35

RESULTS AND DISCUSSION On 1 March 2012, an unusual number of thin white lepidopteran eggs was noted in the forest, attached in large numbers to one side of dead leaves on the forest floor. We assume that these eggs were laid by earlier numbers of Achaea catocaloides moths, but this was not monitored directly as the irruption event had not yet peaked and attracted our attention. Adult A. catocaloides were first observed in early March in some areas of the forest. More moths were then observed as numbers increased in other areas of the forest throughout the month of March. The peak in the area where we estimated density occurred in late March before the start of the seasonal rains. Adult moth abundance peaked from 18–22 March in some areas and from 25 March–3 April in others <3 km away. During these periods, we observed large numbers of A. catocaloides moths flying at various sites widespread throughout the indigenous forest areas (ca. 11 000 ha), spanning distances of ~20 km. Reports of simultaneous irruptions were also received from Kaimosi in Kenya (B. Obanda, T. Achevi pers. comm.) and from Mabira Forest in Uganda (Nature Uganda office, pers. comm.). These observations match previous reports of population irruptions of this moth, when large numbers of adult moths were observed synchronously (Eluwa, 1977; Grubb, 1980, Maisels, 2004).

In Kakamega we did not observe moths in exotic plantation forest areas located adjacent to the indigenous forest patches where we made observations, even though we conducted extensive fieldwork in both natural and plantation forest areas. However, as extensive plantations occur in a patchwork around the indigenous forest, it is possible that moths were present in other plantation areas that we did not visit. We also did not observe or receive reports of caterpillars feeding on crops during this irruption. There was limited defoliation of trees observed as part of this outbreak. Once the ‘long rains’ began (first heavy storms began on the 1 April after a 3 week dry spell) the moths reduced significantly in abundance and were not observed after mid-April.

Estimates of abundance from the transect counts averaged 6.8 (± 3.34, range: 1.9–10.0, N=25 transects) individual moths per square meter. Roosting moth density was estimated at ca. 12.7 (± 4.59, range: 4–23, N=40 replicates) individuals per branch on the trees Bridelia micrantha and Croton megalocarpus. As these estimates are based on multiple replicates from different sites they give a measure of how common A. catocaloides was during this irruption. Scaling up the estimate of 6.8 moths flying per square metre yields an estimate of 68 000 moths per hectare (based on transect count data) with a range of 19 000–100 000 moths per hectare. These values can be scaled up further (using the conversion of 1 hectare = 10 000 sq. metres x 11 888 ha, which is the estimated indigenous forest area) to give a crude estimate of 800 million A. catocaloides moths in this Kakamega Forest irruption (with a range of 22.58 million to 11.8 billion moths). This crude estimate assumes an even distribution of moths throughout the indigenous forest, which may have not been the case. Our estimates may be affected by the propensity for moths to aggregate near paths which are used as flyways. Nonetheless, we note that all sites visited within the indigenous forest by our team had large numbers of moths and similar observations were made in other parts of the forest by several other observers including members of the local guides association and research assistants.

Our estimate of irruption size is based on transect data scores for those moths that could be counted near the ground and on lower vegetation, and that were disturbed while we walked along the transects. It was not possible to count moths roosting in tall trees. Large numbers of moths were observed flying out from tall Croton megalocarpus and Ficus spp. trees at multiple sites. Therefore, the number of moths present as part of this recent irruption is likely to be higher than we have estimated.

36 D.J. Martins, S.E. Miller, M. Cords, M.T. Hirschauer & C.B. Goodale

Irruptions like the one we observed show that populations of tropical Lepidoptera in forests

can reach high numbers rapidly and that these irruptions are occasional features of these wet-dry forest areas’ ecology. Many forest birds and mammals took advantage of the abundant moths, including both insectivorous species like bee-eaters and trogons as well as species that supplement their diet with insects, such as blue monkeys Cercopithecus mitis Wolf 1822 and red-footed sun squirrels Heliosciurus rufobrachium Waterhouse 1842. We observed a total of 14 bird species feeding on the moths in the indigenous forest area (table 1).

Our observations add to the records made over the last few decades of periodic irruptions of the moth A. catocaloides. This is an interesting episodic irruption in the tropical forest areas of Africa. However, the factors that allow these moths to reach such ‘plague’ proportions remain to be understood. Notably, most of the moth irruptions are only recorded once adult moths are visible. Therefore, monitoring of Lepidoptera larvae in forest could help track such irruptions as they build up and offer opportunities for further research into this interesting phenomenon. Table 1. Bird species observed feeding on Achaea catocaloides during the irruption event.

Family Scientific Name Common Name Motacillidae Motacilla agiump Dumont 1821 Pied wagtail

Merops oreobates Sharpe 1892 Cinnamon-chested bee-eater Meropidae Merops muelleri Cassin 1857 Blue-headed bee-eater

Trogonidae Apaloderma vittatum Shelley1882 Bar-tailed trogon Buccanodon duchaillui Cassin 1856 Yellow-spotted barbet Lybius bidentatus Shaw 1798 Double-toothed barbet

Capitonidae

Gymnobucco bonapartei Hartlaub 1854 Grey-throated barbet Monarchidae Elminia longicauda Swainson 1838 African blue flycatcher

Andropadus latirostris Strickland 1844 Yellow-whiskered greenbul Pycnonotidae Pycnonotus barbatus Desfontaine 1789 Common bulbul

Laniidae Lanius mackinnoni Sharpe 1891 Mackinnon’s fiscal Turdidae Cossypha niveicapilla Lafresnaye 1838 Snowy-headed robin chat Muscicapidae Melaenornis edolioides Swainson 1837 Northern black flycatcher Cuculidae Chrysococcyx cupreus Shaw 1792 African emerald cuckoo

ACKNOWLEDGEMENTS Thanks for help with logistics and in general to the Kenya Forest Service, Rondo Retreat Centre, M.N. Mutiso and staff of Nature Kenya, B. Obanda and W. Okeka and guides of the Kakamega Rainforest Tour Guides Association and M. Rosati and L. Helgen. Martins’ work is supported by the Turkana Basin Institute-Stony Brook University, the National Geographic Society, National Museums of Kenya (NMK) and Nature Kenya. Miller’s work on Kenya Lepidoptera has been supported by the International Center for Insect Physiology and Ecology (ICIPE) and NMK. DNA barcoding was provided by the Biodiversity Institute of Ontario, with the support of Genome Canada under the iBOL project. Cords’ work on Kakamega Forest primates is supported by the US National Science Foundation (BCS 1028471), and sponsored by the Center for Kakamega Tropical Forest Studies at Masinde Muliro University of Science and Technology. We thank R. Copeland, D. Agassiz and C. Dewhurst for useful comments on this paper.

Irruption event of Achaea catocaloides 37

REFERENCES Beentje, H. (1994). Kenya Trees, Shrubs and Lianas. National Museums of Kenya, Nairobi. Bennun, L. & P. Njoroge (1999). Important Bird Areas in Kenya. The East Africa Natural

History Society, Nairobi. Berio, E. (1965). Le catocaline africane a tibie spinose de Museo di Tervuren. Annali del

Museo Civico di Storia Naturale Giacomo Doria 75: 181–332. CABI. (2009). Crop-eating caterpillars swarm over Liberia.http://cabiblog.typepad.com/

hand_picked/2009/02/cropeating-caterpillars-swarm-over-liberia.html [accessed 21 April 2012] Craft, K.J., S.U. Pauls, K. Darrow, S.E. Miller, P.D.N. Hebert, L. Helgen, V. Novotny,

& G.D. Weiblen (2010). Population genetics of ecological communities with DNA barcodes: An example from New Guinea Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 107: 5041–5046.

Cords, M. (2012). The thirty year blues: what we know and don’t know about life history, group size and group fission of blue monkeys in the Kakamega Forest, Kenya. In P. Kappeler & D. Watts (eds.), Long-term Studies of Primates. Springer, Berlin. Pp. 289–312.

Dejean, A., B. Nkongmeneck, B. Corbara & C. Djieto-Lordan (1991). The impact of arboricolous ants on an outbreak of Achaea catocaloides (Lepidoptera, Noctuidae) in cocoa plantations of Cameroon, and a study of their associated Homoptera. Acta Oecologia 12: 471–488.

Eluwa, M.C. (1977). Aspects of the biology of Achaea catocaloides Gn. in Nigeria (Lepidoptera: Noctuidae). Revue de Zoologie Africaine 91: 875–892.

Grubb, P. (1980). Observations of Achaea species (Lep., Noctuidae) swarming in the Accra district, Ghana. Entomologists Monthly Magazine 115: 125–130.

Hargreaves, E. (1936). Fruit-piercing Lepidoptera in Sierra Leone. Bulletin of Entomological Research 27: 589–605.

Holland, R.A., M. Wikelski & D.S. Wilcove (2006). How and why do insects migrate? Science 313: 794–796.

Holloway, J.D. (2011). The moths of Borneo: Families Phaudidae, Himantopteridae and Zygaenidae; revised and annotated checklist. Malayan Nature Journal 63: 1–548.

Holloway, J.D. & S.E. Miller (2003). The composition, generic placement and host-plant relationships of the joviana-group in the Parallelia generic complex (Lepidoptera: Noctuidae, Catocalinae). Invertebrate Systematics 17: 111–128.

Larsen, T.B. (1991). Butterflies of Kenya and their Natural History. Oxford University Press, Oxford.

Leston, D. (1979). The natural history of some West African insects. 8. The annual invasion of Accra by noctuid moths (Lep., Noctuidae). Entomologists Monthly Magazine 115: 35–36.

Maisels, F. (2004). Defoliation of a monodominant rain-forest tree by a noctuid moth in Gabon. Journal of Tropical Ecology 20: 239–241.

Miller, S.E. (2007). DNA barcoding and the renaissance of taxonomy. Proceedings of the National Academy of Science of the USA 104: 4775–4776.

Mitchell, N., G. Schaab & J.W. Wägele (2009). Kakamega Forest ecosystem: An introduction to the natural history and the human context. Karlsruher Geowissenschaftliche Schriften BIOTA Report A17.

Pitman, C.R.S. (1931). Capt. C.R.S. Pitman's observations on the excessive abundance and possible migration of a Catocaline moth in Uganda. Proceedings of the Entomological Society of London A 5: 64–65.

38 D.J. Martins, S.E. Miller, M. Cords, M.T. Hirschauer & C.B. Goodale

APPENDIX: DNA BARCODES To facilitate future identifications of both moths and caterpillars, we provide DNA barcodes (Miller 2007) of Achaea catocaloides and several related species from Kenya. Response to the 2009 Liberia event was severely hampered by misidentifications. Achaea catocaloides Guenee: Genbank HM900748, HM900749 (Kakamega), KC170017 (Mpala) Achaea catella Guenee: Genbank JF847875, JF847876 (Nguruman) Achaea lienardi (Boisduval): JF847823, JF847824 (Langata Forest), JN264311 (Kajiado North)