Revista peruana de biología 27(4): 451 - 482 (2020) Ecología y diagnóstico de Enallodiplosis discordis doi: http://dx.doi.org/10.15381/rpb.v27i4.19200 (Diptera:Cecidomyiidae): un nuevo defoliador feroz ISSN-L 1561-0837; eISSN: 1727-9933 Universidad Nacional Mayor de San Marcos con repercusiones directas en la pérdida del bosque seco de Prosopis y los medios de vida en Perú Trabajos originales Presentado: 24/01/2020 Ecology and diagnosis of Enallodiplosis discordis (Diptera:Ce- Aceptado: 06/05/2020 Publicado online: 30/11/2020 cidomyiidae): A fierce new defoliator with direct repercus- Editor: sions for loss of Prosopis dry forest and livelihoods in Peru

Autores Abstract Oliver Q. Whaley* 1, 2 The coastal desert of Peru and Chile is home to Prosopis (Leguminosae: Mimosoide- [email protected] ae) tree species that are exceptionally well-adapted to the hyperarid conditions Consuelo Borda 3 and keystone in dry-forest ecosystems. From 2001 to 2018, Prosopis in Peru have [email protected] 1 suffered widespread defoliation and die-back, with consequent deforestation and Justin Moat Prosop- [email protected] collapse in pod production. This paper reports a new insect plague species of https://orcid.org/0000-0002-5513-3615 is forest in Peru: Enallodiplosis discordis Gagné 1994 (Diptera: Cecidomyiidae) as a fiercely defoliating agent contributing to widespreadProsopis mortality. An analysis Tim Wilkinson 1 [email protected] of E. discordis larval taxonomy, life cycle and plague infestation, following El Niño https://orcid.org/0000-0003-1055-8318 Southern Oscillation (ENSO) 1998/99 is provided. Using distinct lines of evidence, Ana Bravo Sánchez 4 its spread, distribution, and ecology are examined. Over two decades of fieldwork, [email protected] Prosopis forest die-back and loss was observed devastating rural livelihoods and Raymond J. Gagné 5 ecosystem services across lowland regions of southern (Ica), central and northern [email protected] coastal Peru (Lambayeque, La Libertad, Piura). The collapse in production ofProsopis https://orcid.org/0000-0002-3464-757X pods (algarroba, huaranga) and honey was recorded. Supplementary notes pro- Correspondencia vide observations of: (i) plague development, changing land-use and climate, (ii) *Corresponding author biological and physical control of E. discordis, (iii) the moth Melipotisaff. indomita 1 Royal Botanic Gardens, Kew, Richmond, Surrey, (Lepidoptera: Noctuidae) as a concurrent defoliator of Prosopis. TW9 3AE, UK Resumen 2 Royal Botanic Garden Edinburgh, 20A Inverleith Row, Las regiones desérticas costeras del Pacífico de Perú y Chile albergan especies de Edinburgh, EH3 5LR, UK. Prosopis (Leguminosae: Mimosoideae), árboles bien adaptados a las condiciones 3 Asociación para la Niñez y su Ambiente (ANIA), del desierto y con funciones clave en los ecosistemas de bosques secos. Entre el Proyecto Kew-Peru. 2001 y 2017, Prosopis en Perú ha sufrido una extensiva defoliación y muerte regre- 4 Ingleby Farms & Forests, Peru. siva, con la consecuente deforestación y disminución de la producción de vainas 5 Systematic Entomology Laboratory, Agricultural de algarrobo. Aquí, se reporta una nueva especie de insecto plaga del bosque de Research Service, US Department of Agriculture, c/o Prosopis en Perú: Enallodiplosis discordis Gagné 1994 (Diptera: Cecidomyiidae), Smithsonian Institution MRC-168, PO Box 37012, una feroz especie defoliadora que contribuye a la mortalidad generalizada de Washington, DC 20013-7012, USA. Prosopis. Se proporciona un análisis de la taxonomía larvaria de E. discordis, ciclo de vida y la infestación ocurrida después de El Niño Oscilación del Sur (ENSO) 1998/99. Su dispersión, distribución y ecología es examinada utilizando distintas líneas de evidencia. Durante casi dos décadas de trabajo de campo, se observó la muerte regresiva del bosque de Prosopis devastando los medios de vida rurales y los servicios de los ecosistemas en las regiones de las tierras bajas del sur (Ica), el Citación centro y el norte de la costa peruana (Lambayeque, La Libertad, Piura). El colapso en la producción de vainas de Prosopis (algarroba, huaranga) y miel también fue Whaley OQ, Borda C, Moat J, Wilkinson T, Bravo Sánchez A, Gagné RJ. 2020. Ecology and registrada. Las notas complementarias proporcionan observaciones sobre: (i) diagnosis of Enallodiplosis discordis (Dip- el desarrollo de la plaga y el cambio de uso de la tierra y el clima, (ii) el control tera:Cecidomyiidae): A fierce new defoli- biológico y físico deE. discordis, (iii) la polilla Melipotisaff. indomita (Lepidoptera: ator with direct repercussions for loss of Noctuidae) como defoliador concurrente de Prosopis. Prosopis dry forest and livelihoods in Peru. Revista peruana de biología 27(3): 451 - Keywords: 482 (November 2020). doi: http://dx.doi. Algarrobo; ENSO; forest plagues; gall midge; Melipotis. org/10.15381/rpb.v27i4.19200 Palabras clave: Algarrobo; ENOS; plagas forestales; moscas de las agallas; Melipotis. ______

Journal home page: http://revistasinvestigacion.unmsm.edu.pe/index.php/rpb/index © Los autores. Este artículo es publicado por la Revista Peruana de Biología de la Facultad de Ciencias Biológicas, Universidad Nacional Mayor de San Marcos. Este es un artículo de acceso abierto, distribuido bajo los términos de la Licencia Creative Commons Atribución-NoComercial- CompartirIgual 4.0 Internacional.(http://creativecommons.org/licenses/by-nc-sa/4.0/), que permite el uso no comercial, distribución y repro- ducción en cualquier medio, siempre que la obra original sea debidamente citada. Para uso comercial póngase en contacto con: revistaperuana. [email protected]

451 Whaley et al.

Introduction al. 2012). Prosopis in Peru are highly variable with hu- man selection, hybridisation and translocation since the The genus Prosopis (Leguminosae: Mimosoideae) dawn of pre-Columbian history (Whaley et al comprises approximately 45 tree and shrub species, dis- . hereafter, we simply use ‘ ’ to encompass all the tributed across arid and semiarid environments of the Prosopis coastal Peruvian species, forms and varieties. 2019); so Americas, Africa and Asia (Burkhart 1976, Catalano et Prosopis al. 2008), most of which have high economic and eco- The heterogeneous architecture of Prosopis, together logical importance (e.g. Simpson 1977, Pasiecznik 2001, Catalano et al. 2008). Around 39 South American species multiple niches for insect species in arid conditions have a centre of diversity in Chaco (Argentina, Bolivia, (Simpsonwith its prolific 1977, provisionNúñez-Sacarías of nectar 1993). and Althoughfruits provides most Paraguay around 27 species). Around six to seven spe- insects are naturally associated with the tree, due to their prevalence and economic potential Prosopis insects and Peru, with a wide diversity of landraces and local pu- tativecies, are hybrids, found creatingin the arid taxonomic Pacific western confusion side (Burkhart of Chile - 1976, Brücher 2012, Whaley et al. 2019). haveciated often with beenPeruvian categorised coastal Prosopis as plagues species in Peru reported (Díaz Celis176 species 1977, 1995,in Ica and Díaz Piura 1997). regions, A study from of 1991 insects to 1993 asso The coast of Peru is recognised as part of one of the - world’s oldest and driest deserts (Hartley et al. 2005), ura recorded 129 species (Juárez et al. 2016). where plants derive moisture from fog and seasonal An- (Núñez-Sacarías 1993), whilst a site-specific study in Pi Gall midges in forest and Prosopis trees Whaley et al.2010b). West of the Andean mountain chain, dean fluvial influx (e.g. Péfaur 1982, Dillon et al. 1991, Enallodiplosis discordis belongs to the gall midge - around 3200 kilometres, through Peru, north and central icance and role of many species in forest ecosystems Chile.aridity A dominatestrend to hyperaridity the length increases of the Pacific towards seaboard the 18°S for isfamily unknown. (Diptera: As Cecidomyiidae),many Cecidomyiidae where are the small true inconsignif- latitude - the ‘arid divide’. The aridity traverses the Andes to Bolivia and Argentina, to form a diagonal swathe from andspicuous widespread flies they components can easily of beforest overlooked and agricultur (Gagné- biome, Prosopis 1994, Skuhravá 2005), but doubtlessly are significant componentPacific Equatorial of the vegetation. dry forest toIn Chaco;Peru especially, throughout Prosop this- et al. 2016), with many forest species still undescribed is are the dominant is frequently species (Ferreyrathe key arboreal 1987, Whaleyhardwood et (Jaschhofal ecosystems & Jaschhof (see e.g. 2014). Cilbircioğlu Cecidomyiidae 2009, Altamiranobiology is al. 2010a,b, Beresford-Jones 2011, Whaley et al. 2019) varied but many are gall-formers, hence their common where–as phreatophytes–they are resilient to prolonged aridity whilst also adapted to fog capture (Whaley et al. 2010b). Prosopis name; some are fungivorous, free-living phytophages or- south America or ‘huarango’ in southern Peru) are mul- predators. Gall midges may constitute the largest family ti-use species, and trees throughout (frequently human called history ‘algarrobo’ have pro in- of flies (Gagné 1994) with more than 6,590 species de vided essential resources of forage, food and fuel (Beres- scribedLittle (Gagné research & Jaschhof has been 2017). conducted on gall midges ford-Jones et al. 2009). All their biomass can be used and in Prosopis, although a few studies have focused on the many species adapt well to silvopastoral and agroforestry Asphondylia prosopidis) which production (e.g. Roig 1993, Felker et al. 1981, Pasiecznik produces bud galls in P. glandulosa Torr. in south-west et al. 2001). Bioarchaeological studies suggest that South USAmesquite (e.g. van gall Klinken midge et ( al. 2009). Asphondylia prosopi- American Prosopis have played a vital role in the ability of dis is reported in Israel as responsible for the formation people to settle in arid regions, where these species have of ovary galls in P. farcta occurred for at least 8,000 years (Beresford-Jones et al. 2007), and has been studied for potential biocontrol of 2009, 2011, McRostie 2014, McRostie et al. 2017). Today, Prosopis (Park et al. 2009,(Gerling Zachariades & Kugler et al . 1973,2011). Kay In most Prosopis-rich forest in Peru, Chile and Chaco, contin- Prosopis galls ues to be deforested for fuel and agricultural expansion. In in central Chaco (Salta, Argentina), suggested 62% of gall the Ica region of Peru, the few marginal Prosopis forest rel- Southformation America was induced a non-specific by Cecidomyiidae, study of 29 with P. elata, P. icts still existing, are key to biodiversity, ecosystem health nigra and P. ruscifolia hosting three species, with several and man (Beresford-Jones et al. 2009, 2011, Whaley et al. . 2002). Further work in Ar- 2010a,b). However, degradation and climate change-relat- gentina investigated the potential of Prosopis biocontrol . 2019, p: 34, insectunidentified species (Fernandes (McKay 2007), et al reporting Asphondylia aff. 84), and to varying extents, attributable to tree mortality prosopidis as a phytophagous gall midge inducing galls hereined wildfires examined. are now ongoing (Whaley et al on the peduncle and ovary of P. nigra and other Prosopis species. Seventeen gall-forming taxa were recorded on P. The Prosopis species in western Peru –the focus of alba Prosopis pallida Cecidomyiidae (Carabajal de Belluomini et al 2009). (Humb. & Bonpl. ex Willd.) Kunth and . Prosopis limen- in Argentina, of which four to five appeared to be sisthis Benth. paper– This are follows primarily separation classified of asthe two previously Neotropical Prosopis species are known as hosts for synonymised species, and the recognition of Prosopis ju- other Cecidomyiidae species including: Hemiasphondylia liflora as not occurring naturally in Peru (see Burkhart mimosa (in Colombia on P. juliflora Liebeliola prosopidis 1976, Mom et al. 2002, Burghardt et al. 2010, Palacios et (in Argentina on P. strobulifera Tetradiplosis sexdenta- ); ); 452 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis tus (in Argentina on P. alpataco and P. campestris physiology and reproduction, (ii) introduced pathogens Rhopalomyia prosopidis (in Argentina on P. alba, P. alpat- through global trade, (iii) fungal hybridisation, (iv) habi- aco, P. campestris and P. flexuosa ); and- tat fragmentation and degradation (Liebhold et al. 2012, er, all these are gall-forming species, and as such, distinct Mitton & Ferrenberg 2012, Adams et al. 2013, Boone et from the non-gall-forming Enallodiplosis) (Gagné 1994). discordis Howev (in al. 2013, Tobin et al. 2014, Roy et al. 2014, Branco et al. Chile on P. tamarugo and Peru, described here from P. - pallida and P. limensis). troduced Asian beetles Agrilus planipennis (emerald ash borer)2015, Flower and Anoplophora & Gonzalez-Meler glabripennis 2015). (AsianFor example, longhorn in Enallodiplosis discordis, - beetle) are devastating regions of temperate forests - scribed in Prosopis tamarugo in Pampa Tamarugal (Can- was first recorded and de where most research is focused - and Dendroctonus pon- derosa (mountain pine beetle), responding to milder win- al. Prosopis forest was all but ters, assist wide destruction of Pinus contorta (lodgepole chones),eradicated Atacama during the Desert nineteenth-century of northern Chile Chilean (Vargas nitrate et 1989, Gagné 1994). Here, pine) and Pinus ponderosa (ponderosa pine) (Bale et al. 2002, Harvell et al. 2002). In Australian temperate forest, 2001). In 1964 the Chilean government established a Eucalyptus vimina- Prosopisboom (Monteon reforestation 1979, project Estades of 1996,c.100,000 Wisniak ha in &the Garces Pam- lis is suffering die-back over an area of around 2,000 km2 pa Tamarugal (Habit et al. 1981), and –as a management insectof New related South Wales,die-backs with are widespread emerging; infestation of an en- tool– produced a guidebook to insect plagues of Prosop- demic but novel species of eucalyptus weevil Gonipterus is . 1989) in which a cecidomyiid plague of sp., (Coleoptera: Curculionidae) (Ross & Brack 2015). P. tamarugo Contarinia sp.’ (see Fig. 1). (Vargas et al High reproductive rates and dispersal capacity mean described as isEnallodiplosis identified as discordis ‘ Enal- Subsequently,lodiplosis is a monotypicthe species genusproved and new one to scienceof 27 genera and was of are able to cause more damage in water-stressed trees Neotropical Cecidomyiidae, showing (Gagné no close 1994). relation - (Jactelinsects et easily al. 2012, target Haavik native et forests al. (Menéndez 2007), and-

and opportunity for fungal infection 2015). Demonstrablyand hybridisation glo ship to one another or to the formal tribes (Gagné 1994). (Brasierbalised movement 2000). Worldwide, and deforestation studies raise are theshowing frequency die- back in ancient trees, partly attributable to insect attack (Lindenmayer et al. 2012). There is a lack of research into insect plagues in Neotropical dry forest. Prosopis are desert trees referred to as of ‘unsur- -

fungalpassed pathogens, resilience’; but the here shattering we look ofsolely this at resilience die-back as re- sociatedquires consideration with E. discordis. of many possible causes, including The key aims of this paper are to: – E. discordis, Detail the life cycle, taxonomy, and larval stages of – Analyse the interaction and effects of E. discordis Figure 1: (a) the effect of Enallodiplosis discordis on Prosopis aff. in Prosopis trees and foliage, with observations of tamarugo, Pampa Tamarugal, Chile, published in Vargas et al. (1989); distribution and historical ecology, (b) the larvae E. discordis (‘Contarinia sp’.) (×30 original state), attributed to foliar damage of Prosopis leaflets. The larvae appear – Chart the socio-ecological impact of Prosopis die- orange in colour in full sun and pale cream in shaded conditions.). back and pod production, Reproduced by kind permission [Images © O. Whaley] – Assess the relationship of E. discordis and climate change, with ENSO Insect emergence as forest plagues – Suggest methods for physical and biological con- Trade globalisation and climate change have seen for- trol, whilst highlighting areas for further research. est ecosystems under increasing attack from emergent in- sect plagues and pathogens causing forest die-back world- Materials and methods . 2016). Often insect pests are merely Enallodiplosis discordis life cycle.- Observations the most apparent killer, alongside a complex of genetic were made almost exclusively in situ (with no rearing in andwide chemical (Ramsfield interactions et al from opportunistic microbes including bacteria and fungi (see Boone et al. 2013). between 2005 and 2018, using photography and hand captivity) in the regions of Ica, Lambayeque and Piura, responding to fragmented climate-stressed forest, with <1 mm). Monitoring observations were repeated monthly Cause and effect are difficult to pin down, with insects (aslens permitting for magnification by funding). in the Larval field (larvaediurnal/nocturnal and adult size ac- are attributed to: (i) climate change - conducive to insect tivity was supported by repeat photography. Plastic mem- introduced pathogens. Emergent insect plagues in forests

Rev. peru. biol. 27(4): 451 - 482 (November 2020) 453 Whaley et al. branes were used to intercept the fall of mature larvae below infested tree canopies (Fig. 2). The larval pupation were deposited in herbaria: K, MOL, USM. and emergence were observed over 24 hours during pe- gentina. Herbarium specimens collected during field visits Region of Ica, southern Peru (P. limensis) (including riods of one week. Larvae were placed in glass tubes to marginal areas of adjacent regions, Ayacucho and Huan- observe pupation within Prosopis leaf-litter (Fig. 2), with cavelica) 2001–16. adults studied by netting off branches. Illustrations of lar- val development stages and adults were illustrated from fresh material using a drawing microscope. Additional in northern Peru (P. pallida) 2006, 2007, 2012, 2013, information and images were gathered from herbarium 2015–17.Departments of Piura, La Libertad and Lambayeque specimens with use of a scanning electron microscope P. alba, P. chilensis, P. tamarugo

E. discordis ProvinceTarapacá (P. aff. region, alba, P. Elqui tamarugo Province,) 2016. northern Chile ( (SEM)larvae and at the adults Royal were Botanic detached Gardens, from herbarium Kew. Methodology Prosop- ) 2005, 2010, and El Loa foris specimen SEM specimen collections preparation and mounted. was as follows: Larvae from spec- Province of Corrientes and Chaco, northern Argenti- imens in ethanol were dried using a Tousimis Autosam- na (P. affinis, P. alba, P. kuntzei, P. nigra) 2010. Initially, we assessed the intensity of E. discordis infes- dri-815 Critical Point Dryer (Tousimis, USA). The larvae - Prosopis species in Peru have compound bipinnate leaves eswere were mounted covered onwith SEM a layer stubs of platinum with double-sided using a Quorum sticky tation in Peru using a rapid assessment of leaflet counts. tape (Agar Scientific Ltd, Stanstead, UK); exposed surfac pinna. Ten leaves were selected randomly (on the west- mounted specimens were examined using a Hitachi cold ern-mostcomposed side of 2–4of each pairs tree) of pinnae,for presence and 8–15or absence leaflets of lar per- Q150R ES sputter coater (Quorum, East Sussex, UK). The vae (using a hand lens ×10/20). The infestation value was Corporation, Berkshire, UK) and digital images of larvae 0–10, (0 = no larvae observed and 10 = present on every field emission S-4700 SEM (Hitachi, High Technologies and leaf attachment structures were recorded. Prosopis trees with inaccessible branches, esti- Enallodiplosis discordis larval diagnosis.- - mations were made from available leaves and leaf-litter. ages (in Plates 2–3) were taken with a tabletop Hitachi However,leaflet). In as the presence of E. discordis SEM im Heerbrugg microscope with drawing tube. The larval found that a Leaf Cover Index (LCI) became quickly more became useful specimensTM3000. Drawings were mounted (Plate in 1) Canada were made balsam using or Hoyer’s a Wild asubiquitous–with an indicator of consequentialinfection intensity loss and of defoliation leaflets–it (Fig. was mediumEnallodiplosis following discordisthe method direct outlined observations.- in Gagné (1994). Field coverage).16). LCI was The conducted LCI was tested with by 0–10 students classification and specialists of leaf observations of Prosopis condition and E. discordis infes- and–withcoverage (0 a few= leafless minutes dead of training–thetree, 10 = full results foliage produced [normal] tation, were conducted between 2002 and 2015 across less than one degree of discrepancy. the arid coastal distribution of Prosopis (west of the An- des) in Peru. Locations, herbarium specimens and pho- Prosopis species are not considered deciduous. In the department of Ica, Prosopis do not shed and –more recently– the Locus Map Pro™ mapping appli- NOTE: Peruvian cationtographic on an records Android were phone. made The using intensity GPS, and Google activity Earth of Prosopis trees can shed a small larvae on Prosopis foliage was observed, with added not- percentageleaves as a phenologicalof their leaves response (about to 10%) season; between however, April in ing of biocontrol predators. Any other plant species as- andPiura May, and following Lambayeque fruit production (February to March). sociated with Prosopis, were recorded and examined for Also, after several seasons of extreme drought, Prosop- presence of E. discordis. These species included sub-can- is will sporadically shed leaves or even self-prune (pers. opy shrubs such as Pluchea spp., Lycium americanum, Vallesia glabra and forest tree species: Acacia macracan- tha, Capparis spp. and Parkinsonia spp. Crops of adjacent Prosopisobs.). Furthermore, leaves can aslose noted chlorophyll by Díaz (1997), and fall. we The observed cano- industrial agriculture,; including asparagus, avocado, pythat develops after unseasonal a pale yellow rainfall ‘burnt’ in Piura aspect, and Lambayeque,occasionally grapes, and tomatoes were also monitored and exam- referred to locally as ‘tostadera’, where opportunistic ined for E. discordis. Historical distribution data over the mould fungi appear to speed leaf necrosis. Prosopis trees last 60 years was gathered by the examination of her- in these conditions were ignored. Only when E. discord- barium collections of Prosopis from accessions collected is 1950– Prosopis is also caused by Melipotis (Chile), UNICA (Peru) and USM (Peru) (herbaria codes aff.was indomita identified–a known as the pest cause of Prosopisof leaf shedding was LCI after Holmgren2016, held et at al K. 1990).(UK), MOL Herbarium (Peru), PRGspecimens (Peru), were SGO &used. Cuda Defoliation 1994). We in were not able to ignore this contigu- examined for evidence of larval exuviae, desiccated lar- ous plague species, widely prevalent as (see a Prosopis e.g. Deloach defo- vae and diagnostic spots on the leaves. liator from 2001, and a likely contributing factor to the declining condition of the Prosopis until 2007/08 (see Monitoring of E. discordis infestation was done in Peru Appendix for further information, Fig. 14). (with associated herbarium collections) within 105 relict populations of Prosopis, and repeated over the duration of Drone monitoring.- By 2015–16 the ground-tru- the study, other observations were made in Chile and Ar- thed mortality of Prosopis

in Lambayeque was widely 454 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis apparent across the canopy, with Prosopis trees appear- Distribution and climatic niche of Prosopis and Enallodiplosis.- To represent known distribution of E. discordis, we produced a climate niche model for both ing dark grey, leafless, and skeletal amongst otherwise- Prosopis and E. discordis (Fig. 13) to gain insight into eratedhealthy georeferenced species. Using images a Sensefly of mixed eBee™ forest Classic habitat survey to potential impacts and distribution related to Prosop- drone and Pix4D photogrammetric software, we gen is, but not as a vigorous exacting model. For Prosopis: - 11,605 collected specimens and observation records combine with ground-truthed GPS pointP. pallida layers from (Garmin oth- erGLO), species with ( treeAcacia species macracantha identified., Beautempsia This allowed Capparis us to de these by removing duplicates and species not from South velopavicenniifolia a technique, Bursera to distinguish graveolens dead, Colicodendron Cap- America,were downloaded resulting fromin 1576 GBIF specimen (26 May records. 2014). We alsofiltered re- paris scabridum, Cordia lutea, Cynophalla [Capparis] moved Prosopis species widely considered to have been flexuosa, Loxopterygium huasango, Parkinsonia praecox[ introduced to Brazilian cerrado (P. juliflora and P. palli- and Vallesia] glabra) within an open regenerating[ forest] da structure (published in Baena et al. 2017). ) (De Souza Nascimento et al. 2014).

Figure 2: (a) trapping Enallodiplosis discordis larvae, falling to pupate during the night under Prosopis tree canopy using plastic sheet; b( ) third instar larvae, in the morning having dropped on to sheet (rudimentary cocoon in tube inset); (c) technique of trapping adults during early morning - moving vertically-held sheet covered in vegetable oil over leaf-litter;d ( ) larvae fallen on concrete surface where most desic- cate and die, not having leaf-litter in which to pupate; e( ) Prosopis pods (huaranga or algarroba) once gathered in abundance for food and forage (this image 1994). [Images © O. Whaley]

Rev. peru. biol. 27(4): 451 - 482 (November 2020) 455 Whaley et al.

Using Google Earth longer than cerci, aedeagus slightly shorter than the hy- specimens and removed mistaken localities (i.e. those poproct. Ovipositor short, the cerci ovoid and discrete. in the sea or those wildly, we disjunctive)filtered only leaving georeferenced 523, to E. discordis larvae, was which we added 47 records from our collections. We then used these 570 records to run the Maxent model editedNOTE: version The for full ease diagnosis of access. of Enallo- published in Gagné & Whaley (2020), here we include an diplosis: we used our 547 records from Peru and Chile, Larvae discounting(Phillips et al. those 2006, from Phillips Argentina. & Dudik We2008). examined For the The three instars are strikingly different from one an- 19 BIOCLIM (Hijmans et al. 2005) variables, which we were planning to use as our prediction variables. From E. discordis does not migrate at this stage, but begins to the 19 variables we removed nine, which either exhibit- feedother directly (Fig. 5). upon Unlike hatching, the first often instar settling of most on cecidomyiids, the egg case ed geographic disjuncts (sharp changes in values across - the landscape) or were highly similar (Spatially auto- ogy, except for the head with its long mandibles, the fore correlated). We used the 10 BIOCLIM predicting varia- and(Fig. hind 3). The spiracles, first instar and lacksdorsal obvious crest. Thestructural second morphol instar is bles within the Maxent software–employing the default setting (20% of locations were used to test the model’s instar placement to feed (Figs. 3, 4), although it can also performance)–as these have shown to give robust reli- also stationary and often settles directly upon the first- el al. 2012). posed ventrally, and the dorsum has a series of conspicu- move to another fresh leaflet if necessary. Its head is dis ableProsopis results (Phillips pod production.- & Dudik 2008, Between Davis 1995 and ous, long dark setae. The third instar is the crawling stage, 2017, the socio-economic impact of the plague was when, after completing full growth, the larvae drops from gauged by assessing historical pod production from the plant and burrows into the Prosopis leaf-litter. The local authorities and informal interviews with around head is also ventrally disposed, but the body is covered 60 communities. Information was also collated from with sculpturing and has a pair of ventral pseudopods on Prosopis-dependent communities invited to take part in the ‘Huarango Festival’, initiated in 2005 in the city First instar (Figs. 3a, 4a): Length 0.21–0.30 mm. of Ica to celebrate Prosopis biodiversity and products each of the first seven abdominal segments. Colour – shiny translucent, turning pale yellow. Body (Whaley et al. 2010b). We interviewed commercial and ellipsoid, above convex with dorsal longitudinal carina at non-commercial producers of Prosopis - honey, including commercial artisanal operations such syrup, flour and picuous. Head is large with elongated styliform mandi- bles.each Twosegment pairs middle, of spiracles flat below,present, segmentation one pair anterior incons on prothorax, the other dorsally on eighth abdominal seg- Tallanas: La Españolita(Catacaos), and Miskyhuarango, La Perla (Piura), Samaca Santa Productos Maria de OrgánicosLocuto (Tambo (Ica), as Grande), well as Algarrobinalocal Prosopis Heroica beekeepers Villa, body otherwise featureless. and honey sellers. A few families that had migrated to ment. Papillae not apparent at x600 power resolution; urban areas, from rural Prosopis-dependent communi- Second instar (Figs. 3a, 4c, d): Length 0.70–0.82 mm. ties, were also interviewed. The key aim was to deter- Colour – body from pale yellow to light orange, contrasting Prosopis pod with the prominent dark brown setae. Body ellipsoid, con- - historicallymine the seasonal in memory timing and and experience. quantity of In discussion, tic spiracular system and papillar pattern. Head oriented weharvest, also askedbefore whether and following pod gatherers El Niño couldof 1997/98 remember and towardvex above, venter, flat below, with elongate segmentation pair of defined styliform by mandibles.peripneus Prosopis tree insects, or changes, associated with a col- Spiracles of eighth abdominal segment larger than others. lapse of pod production. Additional information was Six dorsal papillae with long thick setae present on all also gathered from the Instituto Nacional de Recursos thoracic and abdominal segments, except two on eighth abdominal segment. Two pairs of pleural papillae present - SA),Naturales and agroindustry (INRENA), parkentomologists. rangers and officers of the most dorsal of each pair with seta similar to that of dorsal Servicio Nacional de Sanidad Agraria del Perú (SENA on thoracic and first to eighth abdominal segments: the- Results and discussion thesetae; four the dorsal-most most ventral with pleural setae seta as long diminutive, as dorsal barely setae, lon the Enallodiplosis discordis – Diagnosis fourger than ventral-most width of withoutbase of papilla.setae. Eight terminal papillae, Adult.- Head lacking occipital protuberance and eyes (Figs. 3c, 4f, g, h.): Length 1.1–2.4 mm. separated laterally and at vertex. Male antennae with 12 Third instar Colour – pale yellow to dark orange. Body spindleform,

- eachbinodal short, flagellomeres, pyriform. Wing each with node R with reaching one circumfilumposteriad of 5 nalslightly segments, dorsoventrally integument flattened, covered with segmentation, verrucae. Head with (Fig.wing 6).apex, Female M -CuA antennae evanescent with beyondonly seven base. flagellomeres, Tarsal claws 4 orientedpair of pseudopods ventrally, with on venter elongate of first pair to of seventh styliform abdomi man- dibles, cephalic apodemes same length as head capsule. claws. Abdominal terga weakly sclerotised, their only ves- Spatula (Fig. 3c) – extruded anterior portion triangular, titureuntoothed, a posterior curved row beyond of setae. midlength; Male terminalia empodia aswith long gon as- the posterior shaft weaker, narrow, of variable length. ostyli completely setulose, hypoproct bilobed and slightly Six dorsal papillae with long setae present on all thoracic

456 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis and abdominal segments, except two on eighth abdomi- Life cycle observations nal segment. Pleural papillae with setae as long as dorsal The inconspicuous nature and small size of E. dis- papillae. Terminal segment with eight papillae: six with cordis–in combination with ground level emergence and setae same length as proceeding dorsal and pleural pa- pillae, two with somewhat shorter setae. Prothorax with of Prosopis trees–has contributed to a lack of research on thiscopulation insect inconfined South America. under the partially obscured canopy lateral papillae, one with short setae, and a ventral pa- pair of sternal papillae; on each side of spatula a pair of Oviposition.- The female E. discordis lays translucent pale yellow to white eggs, oblong capsule in shape (±50 pilla with short setae. Ventral and sternal papillae not µm), barely visible to the naked eye. Oviposition takes place detectable on body posterior of first abdominal segment. on the upper and lower surface of Prosopis Anus well-defined on venter. leaflets (Fig. 6).

Figure 3. Enallodiplosis discordis, larvae. (a) First instar, dorsal (1), dashes show silhouette of egg case below larva; second instar dorsal (2), dashes show silhouette of egg case (upper arrow) and first instar (lower arrow) below larva; head and thoracic segments, ventral (3), arrow indicates head capsule of first instar; last three abdominal segments, ventral (4); third instar, spatula and associated papillae, ventral (5); eighth and terminal abdominal segments, dorsal (6). Scale lines: (1) 0.05 mm; (2–4) 0.10 mm; (5–6) 0.05 mm. (b) E. discordis third instar, dorsal: entire larva (1); thoracic segments (2); sixth to terminal abdominal segments (3). Scale lines: (1) 250 µm; (2–3) 150 µm. (c) E. discordis third instar, ventrolateral: entire larva (1); head and thoracic segments (2), arrow indicates spatula; seventh to terminal abdominal segments (3), arrow indicates pseudopod. Scale lines: (1) 250 µm; (2–3) 100 µm.

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Perhaps in response to climatic conditions –during predation by ants. This larval ‘rain’ is easily observed by hotter months, the lower surfaces can be favoured. The placing a plastic membrane under infested trees (Fig. 2). female walks between leaves along the leaf rachis and pinna before depositing between 50 and 80 eggs on leaf- doing so by a hard surface (concrete, for example), they - accumulateLarvae burrow in great into thenumbers leaf-litter; (Fig. when2d). prevented from ing the female uses leaf selection to reduce egg density. Notably, larvae can change colour, from cream to pro- lets. The larval density is 1–3 per leafletProsopis (Fig. 9), suggest gressive shades of orange pigmentation, with increased 164 larvae per leaf (in Peruvian Prosopis). Under condi- - Thistions equatesof severe to infestation22–44 larvae with per competition pinna; for space, 132– mobileexposure third to sunlight instar struggle (Fig. 7,9). through When sufficientlythis resulting hydrat exu- 9). Larvae emerge after 1–3 days remaining on the same ed, the leaflets (infested with larvae), leak sap, and the egg density can achieve 10–20 larvae per leaflet (Fig. date, and in doing so the larvae become covered in sap. This allows observation of internal orange pigmented fat (Fig. 6) display a translucent pale-yellow colour, with an body as they become transparent (Fig. 4h). internalleaflet. After orange 2–3 peripheraldays the larvae fat pigmentation. (150–200 µm inFrom length) the Pupation.- After reaching the ground, arching back- colour and turn yellow. wards and forwards, larvae bury themselves in the first instar larval position, the host leaf begins to change Feeding and development.- a 12-hour period, the larvae make a small rudimentary place throughout the year, but with increasing intensi- leaf-litter until reaching 15–25 mm deep (Fig. 6). During Development takes cocoon (Fig. 6). After 48 hours the pupae (1–1.2 mm) turn dark orange (with black eyes), then complete pu- Larvae of gall midges have piercing-sucking mouthparts pation, turning dark brown after 60–70 hours. The adult ty as season warms October to December and into April.- hatches after 3–5 days in the leaf-litter. Without leaf-litter uids. Adult mouthparts consist of the dorsal labrum, lat- as a substrate, pupation rarely takes place and the larvae eraland labella,most adult and mouthpartsa ventral hypoproct are capable lateral of ingestingto the labella liq desiccate and die. After emergence, the adult pulls itself Enallodiplosis discordis lar- up through the leaf-litter, leaving a transparent white pu- vae (apparently) derive nutrition from the leaf by perfo- pal case - clearly visible with a hand lens (Fig. 6). rationmaxillary of thepalpi leaf (Gagné cuticle 1994). into the mesophyll using a pair Emergence and breeding behaviour.- of adults from the leaf-litter begins around daybreak, be- of styliform mandibles; possibly favouring access through- tween 05:45 and 06:00 and continues to 08:00.Emergence Females servethe stomata with a (see hand Discussion), lens: it rolls completing up and does development not remain in vary from 1.2–1.6 mm in length, with a red swollen abdo- 6–10 days. The first instar skin change is difficult to ob 8). Cohorts of different-aged larvae appear together on they crawl across the leaf-litter, until reaching a slightly stuck to the leaf as in the subsequent skin changes (Fig.- elevatedmen and positiondistinct shortabove antennaethe surrounding (seven flagellomeres);leaf-litter, usu- ally on a dead leaf stem or peduncle 2–3 cm above the leaflets. In crowded conditions, the larger third instar lar ground (Fig. 6). Newly hatched females, with wings not instarvae crawl (Fig. over 4c), the the first eight and longitudinal second instar rows larvae of short (Fig. dark9a,b - even at times appearing cannibalistic. During the second er positions. By remaining on the leaf-litter, they are less likelyfully expanded, to encounter make the no males attempt in more to fly elevated or crawl positions. to high setae become apparent (400–600 µm); larvae may move extremely slowly on the leaflets, if at all, largely at night. skin changes–they may move to the underside of leaves begin swarming, at times in thousands, to peak in a mat- During the day in hot weather (±35 °C)–and often during (Fig. 9). However, the second instar (Fig. 4) larvae general- ing Thefrenzy wings between of the 07:00male dry and quickly 07:30. afterThey emergence take narrow, to ly remain in the same position on the leaf surface feeding. Under most climatic conditions, following skin change, a cm above the ground, covering 10–30 cm in width and a maximumrepetitive zig-zagof a few flightpaths metres in length. in a restricted Slightly smaller range 5–30 than larval attachment point (Fig. 9). females, the males (0.9–1.2 mm) appear dark in colour, desiccation spot or ring develops on the leaflet from the After the third instar skin change and larval detach- ment, the exuviae (0.6–0.8 mm long) are visible adhered - - iblewith against large recurved the ground antennae when (12 viewed binodal from flagellomeres) above. This moval of the larvae during the third instar skin change, swarming(Fig. 6a, b). frenzy Even inmay large be swarms, observed they at areground almost level, invis by exposesto the leaflet what (Fig. appears 8). Although to be the not remains always of the both case; instar re exuviae (as in diagnosis above), larvae having stayed in who slept under a Prosopis tree, recounted swarming position during the second instar. The third instar can looking across the leaf-litter surface (a local ‘huaquero’, be observed during the day, arching back and forth, de- in the Nazca area, he had never seen this before). Little audibleactivity soundannoyance is heard. at daybreak Males are every attracted day. Despite to the female years - pheromones, and possibly by visual signals of the red ab- taching from the exuviae by flexing the tail in the air and domen. Although not observed, the females probably ex- finally releasing the head (Fig. 4). During the third in sert their ovipositors to broadcast pheromones–as with instar, the the early larvae evening, move wherearound they very arch slowly themselves on leaflets back for all other Cercidomyiidae–and then withdraw the ovipos- anda few forth hours again, (see until below), dropping progressing during dusk to the or leaflet at night– tip itor and cease delivering pheromone. presumably to avoid desiccation from ground heat and

458 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis

Figure 4. Enallodiplosis larval stages. (a) Newly laid egg, (i) first instar larvae at 1–2 days (ii); b( ) First instar larvae at 3–4 days; (c) Second instar larvae at 4–5 days; (d) Mature second instar larvae; (e) Third instar larvae at 7–9 days; (f) Third instar larvae during skin change in fixed position;g ( ) Mobile third instar larvae preparing to drop to leaf-litter; h( ) Third instar larvae covered in sticky leaf exudate allowing view of internal pigmented fat body. [Images © O. Whaley]

Males swarm around the females in small, loose- Foliage can be several metres above the ground in the ly alternating groups (5–15 cm wide) competing to case of pruned trees, or a few centimetres high for un- mate, with copulation taking 2–4 seconds. The female pruned trees. Males do not attempt to follow the female appears to mate only once but is bombarded by males. upwards but remain swarming at ground level. By 09:20, The female remains in position for 5–20 minutes after few females remain on the ground, and some males stay - hovering just above the leaf-litter. The surrounding air - temperature at this stage in summer months is 25–30 lingcopulation until encountering (Fig. 6j) until Prosopis able to treefly with foliage. wings fully ex - panded, after which she flies directly upwards, spiral er than patches of sun. By 09:35, nearly all females are °C; any males still in flight favour the canopy shade rath

Rev. peru. biol. 27(4): 451 - 482 (November 2020) 459 Whaley et al. found on the foliage, selecting the new light-green leaves are carried away by ants, activated by the heat. By 10:20, and branch tip cohorts for oviposition, rather than dark- some isolated individuals of late emerging females are - er mature leaves (Fig. 6). When sufficient foliage is E.avail dis- observed, although the very few males still flying do not Numbers of larvae per tree.- To make a rough esti- cordisable, only defoliating one or two cycle), eggs 10 are or laid more per eggs leaflet; are conversely, found laid attempt to copulate during short flights. when few leaflets are available (towards the end of mation of population density and reproductive capacity of E. discordis in one location in Ica (5–9 May, 2007), a 2) was placed 3.5 me- beon aobserved single leaflet per branch(Fig. 9). (Fig. With 6). shortage By 10:00, of available the number new tres from the trunk under a typical mature Prosopis tree ofleaves–after females on years lower of infestation–fivebranches declines or moreas they females disperse can water-trap(c tray (23×18 cm; 414 cm - up into the canopy, and very few females remain on the opy and observed for four consecutive windless nights. A ground (1–3 per m2 total.40–60 of 160 yr., E.50 discordis cm diameter at breast height [DBH]) can with smaller abdomens. Males are mostly expended and ); those remaining tend to be stunted (having dropped to pupate). final instar larvae were trapped

Figure 5. Lifecycle of Enallodiplosis discordis. (a) Prosopis tree host, with pinnate leaves of 8–12 paired leaflets; (b) oviposition onProsopis leaflet; (c) first instar larvae, often found singly on leaf surface, or up to 10+ larvae per leaflet when few leaves available; (d) second instar larvae with longitudinal rows of short dark setae; (e) leaf necrosis ring formation from larval position;f ( ) second instar larvae during skin change; (g) third instar larvae moving to leaflet tip and then dropping to ground; h( ) on the ground, larvae wriggles slowly into leaf-litter to depth of 15–25 mm; (i) larva pupation in rudimentary cocoon (see Fig. 2); j( ) pupa before eclosion, ventral view; (k) female on ground attracting males for mating;l ( ) males swarm in mating frenzy just above ground, not ascending; m( ) females ascend vertically into the tree canopy, walking from leaf to leaf during oviposition. [Drawing © O. Whaley]

460 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis

Figure 6. Enallodiplosis discordis adult breeding behaviour and pupation. (a) female and male E. discordis; (b) SEM image of male antennae with binodal flagellomeres and nodal circumfilum;c ( ) pupal case in leaf-litter; d( ) pupal case SEM image; (e) female, with dark orange abdomen and short antennae of seven flagellomeres; f( ) male showing long antennae, around same length as body; (g) freshly fallen third instar larva starting pupation (biro for scale), inset shows larvae flexing to move down into leaf-litter for pupation;h ( ) female starting oviposition in foliage around 7.30 am (underside of Prosopis leaflet); i( ) males approach female for mating, second mated female (red arrow); (j) imago females waiting in raised positions on leaf-litter to mate before flying upwards. [Images © O. Whaley, (a) © Ana Bravo].

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2, it can be suggest they might access leaf interior nutrients through upper epidermis stomata. densityGiven and the infection tree canopy above area tray) of aroundmature 80larvae m dropped Enallodiplosis discordis larvae apparently respond assumed that at least 50000 (77295 given equal foliage- strongly to temperature and humidity, becoming active lion per month. This suggests that during the peak larval at night and during high humidity and low temperatures. infestationper night from period a single (4 months tree, equatingper year), to 6 atmillion least individ1.5 mil- This may be a strategy to avoid desiccation, and to feed ual E. discordis larvae could reach maturity on an aver- during times of highest metabolic rate in the Prosopis host. age sized tree. Besides collecting the larvae, 145 adult males and 33 adult females were also trapped, suggest- are most exposed during the day. Prosopis have evolved to ing a male:female sex ratio of around 4:1. The number of maintainThis is clearly a favourable unrelated water to predator potential avoidance; in hyperarid in that desert they larvae reared through to adult emergence, suggests this conditions by opening stomata at night, and during high ratio might vary with temperature -in a warmer environ- photosynthetic activity in the early morning. This obser- ment an inverse ratio was found. vation supports Sudzuki’s (1985) concept of Prosopis hy- Larval movement and feeding.- Observation of lar- draulic lift –a physiology to which E. discordis may have evolved. There does appear to be a relationship with E. over 6 days noted: (i) larvae are most mobile during the discordis feeding times and Prosopis host tree metabo- val movement–(made in Lambayeque and elsewhere) lism. Research in P. tamarugo in Pampa Tamarugal, Chile demonstrated that 35-year-old trees at 04:00 had 80% of undersidenight; (ii) theyto feed move and from moult. their Often diurnal by the positions, second instar, from the stomata open at 84% RH (8 °C), contrasting with 83% the second instar; (iii) they often migrate to the leaflet of stomata closed at 12:00 midday–a time with the hottest desiccate or drop off–depending on its exposure to sun temperature and lowest RH (33% RH / 30 °C) (Sudzuki andlarvae humidity. are compelled Larvae tocan, move, if compelled, as the leaflet move has to feedbegun sev to- 1985). Likewise, the Prosopis sub-canopy percentage RH to the opposite pinna. They move during the night and to >84% RH from around midnight until peaking in the earlyeral leaflets morning, away corresponding from the original with leaflet, lower eventemperatures crossing morning(26 September around 2014, 06:30 Lambayeque) at 91% RH. After rises 09:30,steeply humidity at night and higher percentage relative humidity (RH) (Fig. 7), drops rapidly to <60% RH at 11:00 and to <50% RH from stomatal opening periods, also perhaps with higher leaf >70% RH by 19:15, an hour after sundown (our project the size of mandible stylets and the posture of larvae Tinytag™12:00 midday dataloggers). until around 17:45, when it rises quickly to turgor providing better sap flow. At least in final instars,

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0 A1 day 1 A2 B1 day 6 B2

T # leaflets yellow leaflets green leaflets 1st & 2nd instar larvae 3rd instar larvae Lineal (green leaflets ) Polinómica (3rd instar larvae)

Figure 7. Effect and movement ofEnallodiplosis discordis larvae (in situ on two paired Prosopis leaves). DAY 1: (a1) Second instar larvae in typical position, 1–4 per leaflet, some leaflets attacked have begun to lose chlorophyll;b2 ( ) Leaf recently colonised by two larvae in second instar (yellow arrow) with little leaf discoloration. DAY 6: (a2) Most larvae have moved from the desiccating leaflets, some larvae remain and die or are preyed upon (red arrow), necrotic leaflets are falling;b2 ( ) Leaflets are colonised by third instar larvae, that move to leaflet tips (yellow arrows) to drop to the ground to pupate in leaf litter. Some second instar larvae have moved to right leaf (as indicated). *Leaflets’ changed orientation numbers match leaves, red larvae (top) colour enhanced for visualisation.c ( ) Graph indicating the defoliation of leaflets (ina , b) in relation toE. discordis larval development and feeding movement. [Images © O. Whaley]

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Mechanism for feeding.- The sedentary posture of E. skin changes. However, as the leaf usually desiccates from discordis larva, means the head and mouthparts are con- this point (Fig. 8,9), the feeding appears to take place in cealed beneath the body, effectively hiding observation the same location. Research demonstrates Cecidomyiidae larvae, have evolved salivary proteins that, when inject- ed into the leaf, induce systemic molecular-level changes leavingof feeding. a slight By careful depression removal and of perforation larvae from in leafletsthe leaf itep is- in host plants to produce tissue growth. (Johnson et al. idermis–probablyclear they derive due sustenance to the uptake directly of sap from and/or the leaflets, altera- 2015). We found no easily discernible structural changes - to leaf tissue that might suggest that E. discordis is using pecially, removal of larvae exposes a pale-yellow exudate other chemical messaging secretions to facilitate feeding. thattion ofmay the include mesophilic digestive cell structure. enzymes. In Interestingly, the first instar under es The surface morphology of Prosopis leaves around skin- - change and feeding sites, shows a ridge formation around dence of perforation of the leaf cuticle for feeding during (Fig. 8, 9f). the SEM or light microscope there is no consistent evi the site observable under the SEM

Figure 8. SEM images of Prosopis leaflets at Enallodiplosis discordis larval skin-change sites. (a) Prosopis leaflet (±1.7 mm wide) showing larval skin-change adhesion site with exuviae, necrotic area spreading through half the leaflet. The ridged boundary between desiccation and chlorophyll is visible (white arrow), inset shows leaflet colour; b( ) Close-up of site (±600 µm) on the hairless leaflet underside with high density of stomata; (c) Close-up of ridge at point X on image above, with filaments resembling fungal hyphae across surface and entering stomata; (d) Larval exuviae (±600 µm) on upper leaflet surface with evidence of palisade parenchyma cell decay after third instar larvae skin change; (e) Close-up of larval exuviae with resemblance of fungal hyphae apparently growing from exuviae; (f) First instar larval skin change position, with little evidence of leaf perforation but blocking of stomata;g ( ) Third second instar exuviae sites (photo); (h) Second instar exuviae with suggestion of cannibalism. [Images © O. Whaley]

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project dataloggers). Accordingly, the seasonal temperature nodule sometimes occurs concurrently with E. discordis minimum seen in southern Peru, is moderated in northern infestationIntriguingly, (Fig. 9e) an and unidentified is conceivably red pubescentrelated. These gall-like nod- Peru, where the plague appears to sustain more intensity ules appear as the same colour and size as the female and with somewhat reduced seasonality. The occurrence and might have evolved to deter other females from oviposi- intensity of E. discordis as a defoliant, has been variable tion in areas of high infection. Cecidomyiidae gall-formers over the last few years, perhaps due to unseasonal climate have been shown to be able to induce galls several centi- metres distant their location (Sopow et al. 2003). 2015/16. It is notable that Enallodiplosis appears to respond shifts and the effects of El Niño Southern Oscillation (ENSO) In summary, movement of E. discordis larvae is very re- temperatures at c.5 °C over seasonal averages through much stricted and rarely more than c. ofpositively the cycle to (Takahashi heat, and 2004).that El MoreNino climateof 1997/98 related raised research land is clearly needed. Prosopis leaf pinna. They remain15 largelymm from stationary the leaflet dur on- ingwhich the the day, egg though was depositedmove slowly and when is then necessary–around confined to the Tree resilience and mortality.- Prosopis trees in the Ica region, are partially reliant on fog instar after skin change when they drop to pupate. moisture that is trapped by foliage andDuring drips winter on to months, soil be- and between leaflets–at night (Fig. 7), until the final third - Damage to Prosopis foliage cial root networks to capture this moisture (Whaley et al. Both on the upper and lower surfaces of Prosopis leaf- 2010b,neath the 2019). trees, As seeing a result, seasonal defoliation development (from E. of discordis superfi) lets, E. discordis larvae appear as tiny compressed cap- results in a positive feedback cycle, where less foliage = less fog drip, and the diminishing moisture input is compound- larval movement from a feeding or skin-change position sules (≤1.2 mm), orange to yellow or cream in colour. After shaded, exposed and desiccated, leading to tree mortality. blotch or ring appears (Fig. 8), suggesting the injection of Conversely,ed by sub-canopy any large ground Prosopis heating; trees the that ground grow becomes near water less on a leaflet (exuviae often remain), a symptomatic pale sources, can ‘outgrow’ the defoliation through repetitive turns pale cream, progressively along the branch from the leaf renewal –the water and the high insolation rates sus- newenzymes leaf cohorts that dissipate. that are Over infected. the next Cohorts 1–3 ofdays Prosopis the leaflet leaf- the majority are aborted, with most pods failing to devel- optain (Fig. productivity. 9h). The lackHowever, of precipitation they produce –and few the flowers continued and treelets thena ‘burnt’ quickly appearance become yellow(Fig. 10). (or Leaves cream) desiccate and necrotic, after defoliation (in wind-sheltered conditions)–produces deep infection,falling after depending 3–10 days on (Fig. the 10).climatic The conditionsdying leaflets (related give the to leaf-litter layering (Fig. 10d). However, the majority of foliage moisture content, species, etc.). In the most humid Prosopis have little access to near-surface ground water, conditions, leaves rapidly turn yellow (Fig. 10g), however and after several years of defoliation die back, or succumb in the driest conditions we observed–such as in San Pedro with a failure of hydraulic conductivity and carbon starva- de Atacama, Chile–P. alba leaves remain with a ring around tion (see Sevanto et al. 2014). Tree mortality may be accel- E. discordis larval perforation, turning yellow slowly, over erated by basidiomycete and other fungal pathogens. For - example the polypore fungus Phellinus rimosus, was found star larvae on the same leaves become ‘stranded’ and can on dead branch stumps (Usaca, Rio Poroma, near Nazca, Ica desiccateweeks not and days. die When (Fig. the9). leaves desiccate rapidly, first in region). But with a global distribution, here its association is most likely to be as an opportunistic saprophytic decom- The physical appearance of Prosopis tree foliage dur- ing E. discordis plague outbreaks, appears to be identical to those observed in Chilean Prosopis . 1989) poserA continual (pers. comm. process Brian of Spooner, defoliation RBGK). by E. discordis (and . (1989) guide provides detailed ob- Melipotis see below), gradually debilitates the tree and– (Vargas et al although immensely resilient–the Prosopis tree becomes colour(Fig.1). thatThe Vargascorrespond et al to the positions where the larvae susceptible to drought stress and fungal attack. Branches servation, saying: ‘Leaflets show circularFoliolos blotches presentan of a pale die back progressively (see Fig. 10), even self-pruning, un- manchas circulares de color blanquecino que corresponden dehave sities fixed donde themselves se fija la tolarva suck para the chupar sap’ ( la savia’). (ii)til the beetle trunk holes itself (Cerambycidae)desiccates. The tell-tale appearing signs on confirming all sides Phenology.- Enallodiplosis discordis was recorded oftree the mortality main trunk, are: (i)(iii) branches the splitting being and completely delaminating leafless, of throughout the year (throughout monitoring decade) as a bark on the main trunk, (iv) all round tree, the outer twigs Prosopis - snapping test, produces a puff of wood dust (Fig. 10). cember) in southern Peru, as temperatures increased to a rangeprolific of plague 12–32 in °C and with. During the new the leaf spring cohorts, (October–De numbers It is important to distinguish between the stark visual effect of Prosopis leaf shedding–due to short precipita- tion events outlined–and that of E. discordis-mediated c.of15–37 larvae °C)increased and thereafter significantly declined (Fig.11). with They the continuedonset of the to leaf necrosis. Unseasonal rainfall events (likely climate multiply during the late summer monthsc.6–31 °C).(December–April; Whilst annual change) can cause yellowing of whole tree canopies, whereas, E. discordis infestation yellowing is progres- austral winter (May–September; sive, dispersed, and with cohorts of leaves turning yellow andpeak rarely temperatures drops below are not 13 hugely°C even different in winter in (accordingLambayeque to from the older to the newer leaves (Fig. 9,10). and Ica, Lambayeque experiences much higher humidity

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Figure 9. Enallodiplosis discordis larvae on Prosopis foliage: (a) Larvae of first and second instars, at high density when little foliage remains; b( ) ‘Target’ leaf necrosis rings around larval skin change position (white arrow), most prevalent in more humid conditions; c( ) Close-up of remaining skin change and leaf necrosis; (d) Characteristic ‘half leaflet desiccation’ following larval colonisation in more arid conditions;e ( ) Unidentified red galls found uncommonly with E. discordis, north and south Peru [photo Bosque El Cañoncillo, Trujillo]; (f) Typical leaflet necrosis following larval stages, some larvae desiccated or preyed upon; (g) Bunched brachyblast leaves (P. limensis) desiccate spontaneously; (h) Foliage desiccates and flowers fail or are aborted; rarely forming pods, they exudate gum, desiccate and fall [photos taken in Ica, La Libertad, Lambayeque, Piura – images © O. Whaley]. (For normal pod/flower appearance, see Whaley et al. 2019.)

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Figure 10. Prosopis tree and forest die-back. (a) Characteristic dense upper canopy foliage in healthy tree, with Enallodiplosis discordis yellowing in lower branches (P. limensis, Poroma, Ica, July 2007); (b) Yellowing of canopy after 8+ years of repeated defoliation, re-sprouting with immediate E. discordis infection P.( pallida, Tucume, Lambayeque, Sept 2015); (c) Foliage re-sprout in single branch remaining alive, following 2015–16 El Niño rains (P. pallida, Salas, Lambayeque, Feb 2016); (d) Fallen leaflets accumulating in sheltered conditions, with antlion (Myrmeleontidae) traps P.( limensis, Usaca, Ica, July 2007); (e) Dead trees following 4–5 years de- foliation P.( limensis, Cahuachi, Nasca, Mar 2006); (f) Dead trees after 7–8 years defoliationP. ( pallida, Bosque Pomac, Lambayeque, Nov 2018); (g) NIR image from drone, grey dead Prosopis and red/orange Capparis spp. and Vallesia glabra (La Pena, Lambayeque, Nov 2013); (h) Following El Niño rains, dead Prosopis contrast with other re-sprouting species including Capparis spp., Cordia lutea, V. glabra (La Pena, Salas, Lambayeque, Feb 2016). [Images © O. Whaley, (g) © J. Moat]

466 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis

Leaf necrosis.- The process of leaf necrosis is more From 2001 to 2005 Prosopis tree health declined rap- than likely to include microbial agents, with features idly in southern Peru (LCI decline from 10 in 2000 to <5 such as the formation of a pale ring around the larval in 2006) (see Fig. 11) with localised reduction of infesta- attachment and skin-change points, suggesting fungal tion after 2014, whilst increasing in northern Peru. Our herbarium Prosopis specimens indicate that Enallodiplo- - sis began to take hold as a plague in the Nazca region of gal(or hyphae,filamentous visible bacteria) over the infection. leaf surface SEM and images entering provide the Ica in 2001 (see below), and by 2003/4, Enallodiplosis stomatasome evidence, (Fig. 8c). with Research apparent is neededfilaments to resemblingconclude if funany was found in every tree monitored in the region of Ica, fungal pathogen is intimately linked to E. discordis, or southern Peru. From 2005, Enallodiplosis was discov- whether–at a foliar level–larvae simply provide an entry ered in every Prosopis observed in northern Peru (Lam- pathway for opportunistic microbes. distribution of E. discordis is shown with red dots (Fig. Distribution and Infestation of Enallodiplosis bayeque, La Libertad and Piura). Our current recorded discordis . 2011) we make a rough estima- By 2006–2007, the presence of E. discordis in 13).tion Usingof the thedistribution Geospatial area Conservation of E. discordis Assessment with Prosopis Tool, Prosopis trees (including nursery seedlings) in coastal GeoCATdefoliation (Bachman over of aet minimum al of 4,384 km2 (275 points Peru was found to be nearly universal–occurring in al- area of occupancy with 4 km cell width). most every tree sampled over the distribution (Fig. 11). E. discordis as a Prosopis infestation This included all relict habitats in the department of Ica in 2001, identifying the species in 2003 and reporting as Prosopis is a seriousWe first plague recorded in coastal Peru (Whaley et al. 2010a, b). largely reduced to isolated relict clumps (1–50 trees) in From 2001 until present, in both southern and northern (Fig. 11) that were frequently visited where riparian margins, or communal orchards (huarangales) Peru, Enallodiplosis continues to be widespread. Prior to 5–150 trees (key relicts are: Copara, Coyungo, Huar- - - idence suggest it never occurring as a plague. Neverthe- curi, Poroma, Pozo Santo, Rio Seco, San Pedro, Samaca, less,2001, in it Pampawas overlooked Tamarugal, or misidentifiedChile, E. discordis in Peru, (‘Contarin but ev- angal, Ingenio, Jumana, Ocucaje, Palpa, Pampa de Villa - ia sic Prosopis ble relicts of Prosopis forest (including reserves) in La species, attacking P. tamarugo more than the other four Tingué, Ullujaya, Usaca, Las Trancas). Also, all accessi Enallodiplo- Prosopis sp.’[ species]) (Fig. 1)present was reported (P. alba, P.as chilensis specific, P.to strombu- sis discordis larvae were also found occurring on orna- lifera and the rare P. burkartii Libertad, Lambayeque, Piura and Tumbes. mental trees in Lima. In total, 813 observations were species was reported as a plague, described as becoming made in 105 relict forest patches in regions of south- ‘prevalent in the trees during) (Vargasthe beginning et al. 1989). of spring, The ern and northern Peru. A further 10 observations were and in certain years developing into severe infestations made in Chile and 15 in Argentina. and producing defoliation of Prosopis'.

10

9

8

7

6

5

4

3

2

1

0 4 5 6 7 1 2 3 4 5 6 7 8 0 1 2 3 4 5 19 9 19 9 19 9 19 9 20 0 20 0 20 0 20 0 20 0 20 0 20 0 20 0 20 1 20 1 20 1 20 1 20 1 20 1

Average of Larval counts Average of Leaf cover Index (LCI)

2 per. med. móv. (Average of Larval counts) Lineal (Average of Leaf cover Index (LCI)) Figure 11. Monitoring Prosopis tree health and E. discordis larvae using 813 georeferenced observations from 1994–2015 (nor- thern and southern Peru combined), represented here with yearly average values. Tree health is indicated by leaf cover (Leaf Cover (canopy) Index (LCI) see Fig. 16) and intensity of plague by larvae counts (presence/absence of larvae with leaf monitoring). This provided a consistent picture of declining Prosopis health with increasing larval presence. Since 2015, repeatedly monitored trees were found dead or moribund as linear trend suggests.

Rev. peru. biol. 27(4): 451 - 482 (November 2020) 467 Whaley et al.

Baseline research in Peru.- Although E. discordis about changes in appearance of Prosopis foliage. In Piura, was recorded in Chile in 1966 (2nd following short showers (as outlined) a rapid yellowing it appears never to have been recorded of Prosopis foliage can occur, and be referred by com- in Peru prior to our research. However, March this 1966; species C. couldKlein munities to as ‘tostadera’, and as ‘relámpago’ in Motupe wellin Gagné have 1994),gone unnoticed in the ‘background’ biodiversi- - ty of Prosopis for reasons outlined. There are few base- ported by Prosopis-dependent rural communities. The line entomological studies of Prosopis in Peru, to provide ongoing(Lambayeque). yellowing These of Prosopis were the canopies, only foliage has resulted effects re in conclusive evidence. Núñez-Sacarías (1993) provides widespread worry and confusion in communities with us with a study of insects associated with Prosopis and livestock and algarrobina producers, as the trees in- all Prosop- is-dependent communities, were not able to recognise norecords mention an unidentified of species details. Cecidomyiidae In 2003, speciesBravo Calderón in Piura E.creasingly discordis fail as toan produceinsect or pods. a defoliating Significantly, plague, despite made(CICIU a 11-130-93;detailed evaluation the specimen of insects no inlonger algarrobo exists) (P. with pal- its widespread occurrence, and had no local name for it. lida The characteristic leaf spotting and yellowing, with con- Calderón team evaluated Prosopis forest areas (familiar to the) foliage present in study) Lambayeque, in: northern Peru. The Bravo were not recognised in living memory, and not attribut- - ablesequential to a cause defoliation apart from and a collapsechange in in historically pod production, expe- Motupe (Tongorrape, El Cardo, rienced climate. However, moth plagues were recognised Yocape,35 ‘plague La Capilla),or biocontrol’ Olmos (Cascajal,species were El Puente, collected San fromCris tóbal Chico y Grande) and Salas (Tempon, Dos Cerritos); were ‘pegador de hojas’ (Tortricidae) and ‘gusano defoli- pegador de hojas Olethreu- adorand associated’ (Melipotis with spp.) drought (Fig. 14). and ENSO conditions; these tidaeJuly to family December (Tortricidae)’, 1997. Significantly, as being a principle they report cause only of In summary review, herbarium specimens and inter- widespreadan unidentified defoliation, micro moth present ‘ in 100% of the trees and views provide evidence that: (i) E. discordis, as a species, affecting 75–100% of the foliage (Bravo Calderón 2003). was perhaps present in Peru in 1985, but at very low - that the species is historically unrecognised as a Prosopis portThis studyCecidomyiidae, is also significant, or anything being to prior suggest to the the 1997/98 preva- density, certainly not as a plague and E.easily discordis ignored; had be(ii)- lenceEl Niño. of E. Despite discordis detailed investigation, they do not re come a plague in Ica, and by 2003, could have initiated as from 2005 we recorded E. discordis as the principle and aplague plague in in Peru; Piura, and that (iii) by that 2006, by 2001had developed through- as a misidentified Prosopisplague. Conversely, foliage, in the same areas of Olmos, Motupe and Salas. However, it ubiquitous insect plague species of is again possible that E. discordis–at any stage of life cycle outImportantly, Piura and Lambayeque. E. discordis has only been recognised as and in extremely low numbers–could perhaps have been a Prosopis plague after the ‘extremely strong’ 1997/98 overlooked in such a study. plague of Prosopis (Fig. 11). Further historical evidence.- To further gauge the ENSO, and between 1999 and 2001 in Ica it initiated as a novelty and distribution of E. discordis as a plague, we Enallodiplosis discordis in Chile and Argentina.- In examined historical and contemporary herbarium col- Pampa del Tamarugal (Chile) in April 2010, E. discordis lections of Prosopis. Specimens record symptomatic ev- was recorded at extremely low density (<1 leaf in 10) on idence of the species through leaf spotting, desiccation, P. tamarugo - Corporación Nacional Forestal (CONAF), revealed that E. an and Chilean Prosopis species herbarium specimens discordis had foliage. had little Discussions impact in with recent park years rangers and of was the depositedexuviae and from dried 1946 first to instar 2015 larvae. and held We revisedat herbaria: Peruvi K, not considered as an ongoing plague. In 2011, during E. dis- cordis (as a plague species) prior to 1998. We discov- P. affinis, P. alba and MOL, PRG, SGO, USM. We found no evidence of P.fieldwork kuntzei were in the carefully Argentinian inspected provinces for E. discordisof Buenos infesta Aires,- May 2001 (Rio Poroma, Nazca) and June 2001 (Rio Ica) tions.Corrientes Probable and EntreE. discordis Ríos, species of in situ, inered the evidence Ica region to (Whaley confirm & its Beresford-Jones existence as a coll. plague 2201, in and only found in a single site in the Chaco region, and at 2601, 4901, 026, 062 (K!). In northern Peru, possible extremely low density on P. larvae affinis were and P.identified alba.. This con- E. discordis (appearing as low-density small orange lar- curs with the species presence in the country, alongside vae) was found from 1985 P. pallida collection from Fer- E. discord- is specimens of Brèthes, from Buenos Aires, Argentina. Likewise,the identification the species by Gagné was recorded (1994) of in probable 2012 at San Pedro foundreñafe, with Lambayeque symptomatic (27 Julyevidence 1985; of Percy E. discordis Zevallos from 47 de Atacama, Chile in P. aff. alba (Whaley unpublished). [K! herbarium]). However, a single 2003 specimen was- divia 21). In Chile, the only specimen with evidence of The impact on Prosopis pod production E.Chulucanas, discordis was Piura collected (8 October in 1980 2003; from Rosa Tarapacá Jimenez prov Val- Historical use of pod production.- The most evi- dent indicator of Prosopis forest and tree health, is their pod (fruit) and honey production–stressed trees fail to ince, Camiña (14 November 1980; Lailhacar 59 [SGO! - Local interviews.- Rural communities in both north herbarium]) in non-plague density. P. palli- and south Peru, offered insightful anecdotal information produce pods, with flower abortion and poor pod devel opment. The prolific annual pod production of 468 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis da and P. limensis (see Whaley et al. 2019) in Peru, has year. The harvest has clearly declined sharply due to rap- been (and remains) fundamental to both the subsistence id deforestation for charcoal and agriculture (Whaley et and commercial economy of dry forest communities in al. 2010). We estimate that around 40% of the total pro- duction was lost or consumed in situ by foraging domes- parts of La Libertad (as other arid areas worldwide). On the coastregions of Peru,of Ica, the Piura, nutritious Lambayeque, Prosopis as pod well has as under small- around 156–296 tonnes could have been transported as pinned the development of pre-Columbian cultures over foragetic and and/or wild animals traded in and Ica invertebrates; in the decades suggesting prior to 1998. that at least 10,000 years, whilst the trees have sustained agriculture (Beresford-Jones et al. 2011, Whaley et al. Prosopis forest of northern Peru, where for example, in 2010, 2019). In southern Peru, pods are known as ‘huar- PiuraThis contrasts (areas of quantitivelySan Lorenzo, with Sullana, the comparatively Chulucanas, Medio large anga’, and in the north as ‘algarroba and Bajo Piura) the pod harvests of 1993 to 1995 had an rural communities have remained dependent on this an- annual commercial production of 6,800–12,600 tonnes of ’. Despite the fact that Prosopis trees in Piura Prosopis sincenual resource,1999, due there to interrelated is little published disruption data ofto climatic,quantify pods (Díaz Celis 1995). Some large cultural andpod productionpolitical change. in Peru; On no the figures north are coast, apparent bian- alsocan produce used. A managedup to 300 plotkg of of pods algarrobo per year (Prosopis (Grados pallida & Cruz) nual production (one large, one small) is used for forage, 1996) and an average figure of 46 kg of pods per year is but also for human consumption, processed into a range couldThe produce actual 16500pod production kg/ha/yr in is Piura far larger–by(Díaz Celis several 1995). orders of magnitude–than the commercialised reported coffee substitutes. In times of abundance, the pods are of products including flours, syrups, confectionary and - ed in informal unregistered ways, or consumed in situ as or conditioning horses and livestock in the departments figure, as pods remain unharvested in remote areas, trad used as a premium quality animal fodder for fattening wild or domesticated animal forage. A pod production es- example, a crop was purchased for Lima police horses average of 46 kg of pods per mature tree, multiplying by (pers.of Ica, comm. La Libertad, Felix Quinteros) Lambayeque and in and Piura Piura. used In to Ica, fatten for thetimate number was made of trees for at Subregion estimated II averageLambayeque; densities using from an three Prosopis ecosystems, to reach surprisingly large same purpose. The pod crop is stored during the winter monthsfighting inbulls, dedicated even exported clay-sealed to southern storage rooms Ecuador or for‘algar the- roberas figureIn theof 204,138 Ica region tonnes the (Proyectopod harvest Algarrobo collapsed 1992). rapidly by smallholders, or by itinerant families harvesting on from 2001, to culminate in 2005, in complete pod pro- behalf of’ (Díaz owners, Celis or 1977, from 1995),state land having (following been gathered expro- duction failure south of the region (Santa Cruz, Palpa priation of hacienda land during the Reforma Agraria of and Nazca), with no Prosopis pod products available. In 1969). State land –nominally at least– was once regulat- the Ica valley, previously highly productive Prosopis trees ed by the state through the Instituto Nacional de Recur- San Jacinto and San Pedro) (see Fig. 11, Fig. 12d) failed de Agricultura) following a fee-based concession and re- to(such produce as those a harvest. in marginal Only a dunes few isolated of Pampa individuals Villacuri, sos Naturales (INRENA; now decentralised as Ministerio informal markets, we spoke regularly to several families Santiago de Ica). Flowering was aborted, with remain- inporting the Ica mechanism. region who Although paid for thisconcessions was often and flouted reported with produced any pods at all (such as in Guanaco, Ocucaje, pod harvests by the sack. Throughout the pod season, Prosopis) honey, and lo- prior to 1999, corrals of pigs, sheep or goats were nearly caling marketflowers stalls devoid could of nectar. not obtain In 2006, any afterlocal generationsbeekeepers always found under any Prosopis trees and forests near ofreported supply no(pers. flow obs.). of ‘huarango’ By 2009, (pods were found only in dwellings (pers. obs.). a few urbanised forests of Ica such as the Angostura. It became possible to accurately record the phenology and Quantifying pod production prior to 1997/98 Prosopis pod production in the Ica region is ENSO.- a network of producers during the annual Huarango Fes- quantificationtival, established of thisin 2005 collapse (Whaley in pod et productional. 2010b) and through now in its eleventh year. ofsmall forest compared relicts before to that and of Piurasince the and post-colonial Lambayeque, peri due- to the desert confined riparian oases. 2010, and Beresford-Jones deforestation By 2006/07 in northern Peru the Prosopis pod col- et al. 2011). Pod prices are dependent on the harvest lapse was evident, even in areas such as Tambogrande, od (Díaz Celis 1995, Whaley et al Piura –a stronghold of forest pod production. Santa María de Locuto, one of the largest consumers of Prosop- dependingquantity and on the the quality. point of From sale, 1994season to and1997 year a standard (Fig. 2). is pods for commercial purposes, in order to continue sack of pods (18–20 kg) was sold for 5–20 soles (PEN) production was compelled to purchase pods from as far (100 pounds or 45 kg)–a more common unit in northern away as Chulucanas –over 20 km distant– due to lack Peru.In productive Collated yearsfrom podsextensive could forest be sold surveys by the and ‘quintal’ inter- of production from its surrounding forest (pers. comm. views, we estimate that during the decade up to 1998, company director). Prosopis pods in Ica Pod Production post-1997/98 ENSO.- Both the was between 259–492 tonnes per year during a good Ministry of Agriculture and communities dependent on theyear, total and fluctuating only around productivity 50 tonnes ofor less during a poor Prosopis forest in Piura, reported pivotal shifts and col-

Rev. peru. biol. 27(4): 451 - 482 (November 2020) 469 Whaley et al. lapses in pod productivity around the two ‘very strong’ al. 1987, Takahashi 2004, Cai et al. 2014). Heat spikes, - rainfallEl Niño inevents this arid of 1982/83 desert region (with is published 20–200 mm, figures) whereas and during El Niño of 1982/83 and 1997/98 saw the tem 1997/98 (Fig. 12) (Díaz Celis 1995). A normal annual producingperature in prolonged Piura and droughtLambayeque conditions. peaking Likewise, at 5°C over in the average, with La Niña following the 1997/98 El Niño Niñoboth 1982/83‘very strong’ saw El rainfall Niño asevents follows: registered Chulucanus exceptional >4000 drought until 2005 (Servicio Nacional de Meteorología e rainfall with over 3,000 mm in Piura and Lambayeque (El Ica the 1997/98 El Niño was followed by a period of 3735 mm, Piura 1802 mm (see Takahashi 2004), and - Januarymm, Piura to April2147 1998,mm; andareas El around Niño 1997/98 the towns Chulucanus of Olmos, Hidrología del Peru [SENAMHI]). lis 1995) reveal that between 1984 and 1997 in both Ica Piura and Tambogrande were reported to have received Interviews and Ministry of Agriculture data (in Díaz Ce- over 4,000 mm of rain (Ordinola 2001). ductivity cycles–the production of pods and the rural live- Interviews with the most elderly have suggested that lihoodsand northern that depended Peru–although on them, fluctuating were sustained with normal (Fig. 12c). pro between 1925 and 1982, the region experienced rather consistently dry conditions (borne out by sea surface produce a temporary collapse in Prosopis ofTherefore, 1982/83 evidence (see Fig. suggests 12a, b). thatThe ‘veryarrival strong’ of heavy El Niño rainfall can pods, as in El Niño convertedtemperature to Elscrub Niño or indicator regenerated Zone into 1–2) forest’. and thatThis aftercon- - El Niño of 1982/83 much of the ‘deforested plains were and flooding coincide with pod ripening and the fallen pods 1925/26, 1982/83 and 1997/98 as ‘very strong’, and the soildecay humidity rapidly. andHowever, released after fertility El Niño (Fig. 1982/83 12). pod produc mostcurs with extreme multiple events analyses over the that last class century the ENSO (e.g. Quinncycles ofet tion recovers, and is boosted in subsequent years with high

Prosopis pod (algarroba) annual production 1980-85, 2.500 Prosopis pod (algarroba) annual production 1980-1990 Lambayeque - Piura (Ministerio de Agricultura 1987) subregion II Lambayeque (Proyecto Algarrobo 1992)

12000 1.972 2.000

10000 9724

s d

o s 8137 p

d 1.500

f

o 1.352

8000 o p

) f Major ENSO event 1982-83 T o

) m ( T

s m 991 ( 6000 e

n s 1.000 903 n e o n T n 738 o

T 654 4000 599

500 2000 1600 249 1001 88 128 341 19 0 0 1981 1982 1983 1984 1985 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 year year

Prosopis pod (tonnes) commericialised - registered in Forestal y Fauna, Prosopis pod production in selected huarangales of Ica Direccion Regional Agaria de Piura 1993-96 (Diaz & Cuba (1998), (estimated av. decadal production (kg) from mulitple surveys and interviews) Proyecto Algarrobo INRENA) - largly due to deforestation until 2000, thereafter E. discordis 35.000 100.000

90.000 4.500 30.000 4.079 80.000 4.000 3.531 25.000 70.000 3.500 s d

3089 o

3039 60.000 p

) 3.000 20.000 T g ) k m ( (

50.000 t

s 2.500 e 2.244 2.304 g h

n 2.173 2141 15.000 i e n w o 2.010 1.936 40.000 2.000 T T

1.500 1.415 10.000 30.000

1.000 930 20.000 5.000 500 373 10.000 approx. weight (kg) dry Prosopis pods harvested (by location) 0 0 0 1993 1994 1995 1996 1970's 1980's 1990's 2000 2005 2010

San Lorenzo Sullana Chulucanas Medio y Bajo Piura San Pedro La Huega Orovilca Cachiche San Jacinto Comatrana Santiago Guanaco Santa Vicenta Guadalupe Villacuri total production

Figure 12. Prosopis pod production P.( pallida = algarroba, P. limensis = huaranga). (a) Prosopis pod (algarroba) annual production (mT) 1980–85, Lambayeque and Piura (Ministerio de Agricultura 1987); (b) Prosopis pod (algarroba) annual production (mT) 1980–90, subregion II Lambayeque (Proyecto Algarrobo 1992), red arrows indicate the 1992–83 El Niño event; (c) Prosopis pod (algarroba) commercialised and registered in ‘Forestal y Fauna de la Dirección Regional Agraria de Piura’ (mT) 1993–96 (Diaz & Cuba (1998) Proyecto Algarrobo INRENA); (d) Prosopis pod (huaranga) production (kg) in selected woodlands of Ica Region derived from estimated approximate average decadal production (kg) from surveys and interviews 1970s–2010.

470 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis

This 1982/83 scenario, contrasts completely with a stock forage (or pannage) in Prosopis forest (and ‘algar- steady decline and collapse in pod production in all areas robales of Prosopis distribution on the coast of Peru from 2001, fol- producing around 25% of ‘caprino’ (goats) in Peru in - ’) are unavailable, indicative figures include Piura In contrast to many arid areas, where goats can be Melipotislowing the aff. 1997/98 indomita El Niño(Lepidoptera: (Fig. 12d). Noctuoidea) This decline plagueis con 2006 (MINAG–DGIA). highly detrimental to vegetation, evidence suggests that current with the two powerfulE. discordisdefoliating that agents: sustained. firstly, the goats (and desert sheep) can maintain and regenerate thatAlthough declined; Prosopis and secondly, is a phreatophyte, it is probable that Prosopis forest in Peru (Piura), in that they facilitate ger- a plague trigger is related to unfavourable water balance mination and seed dispersal (Perevolotsky 1990, 1991). resulting in increased sugar content of foliage (see Kulman Prosopis 1971 in Ueckert 1974). Also, climate change induced stress dry leaf-litter. Perevolotsky (1990) found that goat herds is a factor with little baseline research in desert Peru. Significantlyin Piura, increased during inthe size dry during season, the they severe forage drought of It should be mentioned that the possibility of drought conditions being to blame for defoliation, can be dis- 1982 (prior to El Niño), indicating the value of dry forest missed, in that other tree species in Prosopis ecosystems leaf-litter as qualityE. discordis forage. has an obligate relationship continued to thrive, including Acacia and Capparis spe- with Prosopis leaf-litter to complete its lifecycle (see Fig. cies, Cordia lutea, Pluchea chingoyo and the sub-canopy 5), theGiven role that of forest herbivores may be critical to its reg- Vallesia glabra (see Baena et al. 2017). ulation. In Peru dry forest, goats and sheep occupy an Fundamental Change following 1997/98 El Niño.- white-tailed deer (Odocoileus virginianus). The Cronista To understand the novel appearance of E. discordis (and ecological niche previously filled by the once widespread Melipotis), we note fundamental change to the Prosopis, of northern Peru and Ica as running with huge herds ofPadre deer. Bernabé As well Coboas having (1582–1657) a role in reportsforest disturbance the forests 1997/98 (Rein 2007, Cai et al. 2014) including ground- previously performed by megafauna (such as the South water.environment Water-tables following were the raised unprecedented over a space El of Niño a few of American ground sloth (Scelidodon chiliensis) found in days by 10–30 metres both in Piura and Ica. Further- northern coastal Peru at least until 9000 (see Hubbe more, artisan wells used for several generations in Piura et al. 2007). The role of goats and sheep in regulation of E. discordis, as a plague, should not be ignoredbp (see sup- to saline, or mineralised referred to ‘metallic tasting’, plementary notes below). The on-going situation pre- leadingand Lambayeque to land use were and ruined, livestock changing change. from Biologically drinkable in sents a feedback: where collapse of Prosopis pod forage Northern Peru we observed extensive ‘blanket’ growth of sees a reduction in forest-ranged livestock, resulting in Luffa operculata (also noted by less consumption of Prosopis leaf-litter and allowing E. Momordica discordis to proliferate uninterrupted. charantiaCucurbitaceae climbers; - Ferreyraered Pseudogynoxys (1993) after cordifolia 1982/83 (Compositae), El Niño ) and all acting as lianas smothering (introduced), Prosopis as wellforest. as Thisand theeffect orange-flow is perhaps Conclusion We described E. discordis plague in Prosopis in south- compounded by atmospheric CO2 fertilisation (Laurance et al. Prosopis trees were smoth- ern Peru from 2001, and by 2005 in northern Peru. The ered contributing to their mortality (see Fig. 10). 2004). Eventually many these regions as a widespread defoliant. Our evidence sug- As detailed, -reliant communities reported Prosopis gestsspecies it iscontinues a contributor to be to active widespread and ubiquitous die-back todayof Prosopis in all. We were able to gauge the extent of the Prosopis die-back, a collapse in pod production for the first time in living a steady decline from 2003, with 80–90% Prosopis tree analysis (including NIR and Red edge imaging), making 37 mortalitymemory (Fig. by 2016 12), specificallynear Motupe, in Lambayeque Pómac and Salasthere (seewas used an SenseflyProsopis eBee Classic relicts ™and UAV reserves drone for supported broad-scale by Baena et al. 2017) (Fig. 12g). In Prosopis forests around ground-truthed data and plot observation with high reso- Olmos, rural communities reported a single large harvest lutionflights remotein key sensing images (Baena et al. in 2000 and thereafter, a rapid decline until 2004–05 Prosopis mortality (Fig. 10). when pod production collapsed by over 95%, with early 2017); in many - areasRange we confirmed expansion 80–90% or introduction.- Our additional ob- trict around Mano de León). servations in Chile and Argentina, suggest that E. discordis reports of unidentified plagues (pers. comm. rural dis is widely distributed and associated with several Prosopis Changes to Prosopis forest livestock manage- species. Notably, in Pampa Tamarugal, Chile–the region of Recent decades in Peru have seen radical so- ment.- E. discordis ‘became prev- cio-economic change for rural coastal communities. alent during the beginning of spring and in certain years Access to community forest land has been increasingly developedearliest identification into severe as infestationsa plague– producing defoliation blocked by industrial farming and urbanisation. Itiner- of Prosopis . 1989) (Fig. 1). We can hypothe- ant herding of goats and sheep through dry forest is in decline as a way of life, with reductions of herds season- semi-permanent’ (Vargas changes et al conducive to E. discordis plague ally through Prosopis dry forest (see Perevolotsky 1990, size that El Niño 1997/98 in Peru, triggered extended and- - cient climatic and ecological regulation to stem. conditions (that exist intermittently in Chile), with insuffi Popescu 2013, MINAG–DGIA). Although figures for live Rev. peru. biol. 27(4): 451 - 482 (November 2020) 471 Whaley et al.

There is also an outside possibility of assisted migra- discontinuities and conditions, which our model does tion from Chile, through a transport mechanism–easily not include. It could also suggest that the plague is not achieved via the stream of large vehicles moving along greatly controlled by climate variables. This is particu- the Pan-American highway–providing a connection larly true for the climatically distinct outlying Argentina localities which are predicted with extremely low values should be able to the resolve this, and other dispersal (below 0.01). This is not really expected–as the Prosopis through Tacna ‘aridity barrier’. DNA population studies niche model is very robust–and is therefore suggestive that either the E. discordis as a plague (or as normal bi- Niche model for Enallodiplosis discordis.- For fur- and provenance questions. odiversity) has not yet occupied its full niche, or, that ther exploratory insight, we ran a niche model, using a climate is not the only (or strongest) factor determining known distribution of both E. discordis (Fig. 13) and distribution within the Prosopis host distribution. Prosopis species in South America. Interestingly, the niche response (prediction values) for the E. discordis The precipitation variables contributed most to the plague localities are low (>0.6 on a scale of 0–1), suggest- - ing that the model is not predicting well. ditions, with exceptional rainfall, spikes in heat, humid- itymodels. and Prosopis We can postulate that the 1997/98 ENSO con This may be due to narrow distribution of observa- expanding the niche without biological regulation (see Prosopis relicts, or to desert landscape below). productivity, could be a trigger; rapidly tions confined to

Figure 13. Niche models for Enallodiplosis discordis and Prosopis tree genera (c. 39 species) in South America. The Prosopis niche with high to medium predictions are dark to light green, and that of E discordis shaded red (cut out). Records of E. discordis occurrences (mostly as plague although not Argentina or Chile), are indicated by red dots andProsopis voucher collection localities blue dots. Pink areas represent less robust predictions for theE. discordis niche areas and are generally not optimum niche areas for naturalProsopis distribution. Notably within these pink areas several occurrences of E. discordis were found on ornamental Prosopis trees. The inserted image (right), is shown to highlight aridity, with light to dark brown being lowest rainfall and green highest.

472 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis

It is conceivable that this could see rapid adaptive se- 1997/98 with compounding climate change, appears as lection of E. discordis into a more virulent strain to reach a ‘perfect storm’ scenario, where Prosopis, already under these niches. This is a simplistic niche analysis but re- drought stress, sustained unimpeded attack in degraded veals patterns that warrant further investigation. Under- forest, without the herbivore regulation of leaf-litter con- standing the transport vectors for assisted distribution also needs research. The plague should be carefully mon- development of nectar-rich habitat (such as Waltheria itored and evaluated throughout South America - espe- ovatasumption) to sustain(see below). biocontrol Subsequent agents, droughtsthat were prevented impeded cially in arid areas of Chaco and Argentina. usage (that rose exponentially after 1999 (Fig. 14)). ENSO trigger and debilitated habitat resilience.- by increasing agricultural intensification and insecticide The triggering of E. discordis

as a plague, following ENSO

Figure 14. Melipotis moths and Prosopis woodland activity: a( ) Melipotis larvae in diurnal hidden roost under plank next to trunk of Prosopis host (1 Sol coin scale, 2006); (b) Melipotis larvae droppings in trunk cleft, with desiccated larvae after defoliation;c ( ) Adult moth Melipotis aff. indomita, Lambayeque; (d, e) Melipotis aff. indomita, Ica region; (f) Melipotis moth foraging for Prosopis flower nectar at night, Ica; g( ) Livestock herders traditionally fatten goats and sheep on Prosopis pod throughout Peru (Topara, Chincha); (h) Huarango (P. limensis) surviving in the domestic settings (Santiago, Ica);i ( ) Harvesting Prosopis pods for food and forage (1994); (j) Following Prosopis decline in pod productivity charcoal burning became widespread. [Images © O. Whaley, (g) © Claudia Luthi]

Rev. peru. biol. 27(4): 451 - 482 (November 2020) 473 Whaley et al.

Research is needed to determine the role of opportun- and industrial agriculture insecticide use increased (in istic fungal saprobes accelerating leaf necrosis, following P. peruvianus wasp popu- perforation by E. discordis (see Fig. 8), and exploiting fa- lations monitored had been wiped out, leaving only the vourable climatic conditions. Tree fungal pathogen out- mostadjacent isolated fields), colonies. by 2005, We most assume that being hidden breaks have increased widely since 2000 and are already during the day, M. aff. indomita larvae were less subject a recognised effect of climate change and increased glob- to insecticide, enabling their plague-status proliferation, al movement (see Brasier 2000, Fisher et al. 2012). compounded by a lack of the key biological control agent. Tipping point?.- role of Prosopis 1. Melipotis as a plague ofProsopis trees trees in the ecosystem, the die-back is also indicative of We recorded the moth M. aff. indomita causing wide- threshold breaching withGiven tipping the keystone points (see Holmgren et spread defoliation of Prosopis in the Ica region over the pe- al. 2006, Reyer et al. riod 2001–07, during which time its dominance declined many areas are seeing Prosopis dropping out of the forest and was replaced by the new plague, E. discordis. Melipotis 2015). In Ica, Lambayeque and Piura,- moth species are well-documented defoliating plagues of ests converted to charcoal (see Baena et al. 2017, Whaley Prosopis through arid areas of North and South America system completely; ancient trees are dying and dead for- (Brown 1945, Ward et al. - land. Where forest remains, Prosopis mortality releases siana, M. indomita (Walker 1858) as a plague of P. juliflo- nutrients,et al. 2019, allowing p. 34), with other consequential forest species expansion (such as of Acacia farm ra var. glandulosa 1977, Deloach 1994): Prosopisin Loui macracantha, Capparis avicenniifolia, Capparis scabri- pallida da (Colicodendron scabridum), Cordia lutea, Pluchea spp. Texas, M. indomita (Cockerelldefoliation in causing Brown 58% 1945); mortality of in P. Vallesia glabra and the introduced invasive Tamarix aphyl- glandulosa(Kiawe), with in foliage Hawaii reduced 1969 (Odaby 95% and (Ueckert Mau 1974); 1974). in la - In South America, Melipotis species were recorded as a sis of arid systems having alternative vegetation states ) to thrive (with sufficient groundwater). The hypothe Prosopis plague in a wide range of countries, notably: M. ochrodes in Puerto Rico 1936, Chile 1987 and Argentina (Holmgren & Scheffer 2001)–is compelling. And here, the P. flexuosa and P. “mightytriggered midge” by single is also events–including propelled by aman-made very strong climatic ENSO chilensis in Argentina (Cates & Rhoades 1977 in Simpson change and degradation. With profound changes in the (Córdoba)M. trujillensis 1999 (Mazzuferi and M. 2000);walkeri onseverely attacked P. world’s oldest desert forests, and a cultural and ecological chilensis - extinction taking place, it is time to act. gion,1977); Chile, Melipotis species are well-documented as a plague of (Klein several & ProsopisCampos species1978) in reducing Chile. In productivity. Iquique re Supplementary notes They are “nocturnal and remain grouped together inside Here we provide practical guidance for careful man- tree trunk cracks, underneath salt crusts and in leaf-litter agement: (1) Plague development and loss of biocontrol; duringIn Peru the day” Melipotis (Vargas moth et al. species 1989). can be referred to as (2) Melipotis as a plague of Prosopis; (3) Distinguishing- ‘gusano defoliadores’ (defoliating grubs) (Fig. 14), and Melipotis and Enallodiplosis discordis defoliation; (4) normally remain regulated in low numbers as part of Physical and biological control of Melipotis; (5) Biolog healthy Prosopis forest biodiversity. Melipotis as a plague ical control of Enallodiplosis discordis; (6) The role of of Prosopis agentlivestock for Prosopis. in regulation of Enallodiplosis discordis; (7) Note on Enallodiplosis discordis as a potential control Celis (1997) has and been Bravo recorded Calderon in Piura (2003). and LambayequeAlthough no 1. Plague development and loss of biocontrol. by Díaz Celis (1977, 1995), Núñez-Sacarías (1993), Díaz in Ica and Piura regions (1994–2001), by November Following the very strong 2003,widespread we recorded defoliation, was observedinfestations during in fieldwork in 2000/01 La Niña, interviews with small farmers in the Melipotis Prosopis the Ica (and Nazca), that became widespread by 2005 Ica region (2005–08), provided 1997/98 insight. El Niño, From and 2001,weak and resource competi- they experienced a series of intense insect plagues, in- tion with . cluding red spider mite (Acari: Tetranychidae) in Lima E discordis Melipotisdeclined plagues by 2008; are perhapstriggered due by tounfavourable water beans (Phaseolus lunatus) and ‘culi’ (Anthonomus spp.) balance resulting in elevateddefoliation. foliar Evidence sugar concentrations suggests that in cotton (Gossypium spp.). Insect pests developed to (Kulman 1971 in Ueckert 1974), this would concur with such intensity, that many small farmers felt compelled to drought conditions of the period. take out loans to pay for insecticide. At the same time, Enallodiplosis discord- 2. Distinguishing Melipotis and Enallodiplosis is (recorded in herbarium specimen vouchers in 2001), discordis defoliation andwe observed concurrently, the first widespread outbreaks outbreaks of of Melipotis aff. Melipotis larvae are found in Prosopis as a normal indomita (Lepidoptera: Noctuoidea) causing defoliation healthy association (providing forage for woodpeckers, of Prosopis. Biological control agents also proliferated and wasps for example). However, Melipotis infestation as expected. The key predator wasp of Melipotis larvae– as a plague in Prosopis - Polistes peruvianus ence of diurnal larval roosting sites at the base of trunks into huge colonies of nests on cliffs and lower horizontal (see Table 1 and Fig. 14),, is easilyand by confirmed observation by theof larvae pres branches of Prosopis (Hymenoptera: Vespidae)–developed - riparian valleys) (Fig. 15). However, as both smallholder (alongside the agricultural fields of climbing trunks at dusk. Diurnal roosts contain from sev 474 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis eral hundred to several thousand larvae (in proportion to 4. Biological control of Enallodiplosis discordis canopy size). Melipotis larvae are photophobic and crawl rapidly to dark recesses when exposed. Melipotis larvae the high insect diversity of Prosopis, only a few biocon- (in P. limensis in Ica) had preferential selection of young trolDespite species hundredswere recorded of hours feeding of field on E. observation, discordis larvae. and leaves in the outermost leaf cohorts. Once the newest These were: Chrysoperla spp. (Neuroptera: Chrysopidae) leaves have been consumed, the rest of the foliage is de- - voured in one to two weeks (Fig. 14). The diagnostic pat- bird) larvae (Fig. 15a,b) with adults including Hippoda- tern of Melipotis defoliation can easily be distinguished mia‘lacewing’ convergens larvae; and several Paraneda species pallidula of Coccinellidae (Fig. 15f,g), (lady and from E. discordis (Table 1), the key features of Melipotis Cycloneda sanguinea. The being: (i) leaves reduced to naked leaf rachis with few or ladybird P. pallidula is the species most associated with with droppings of Prosopismost recently, in Peru, in Lambayeque especially in areas without heavy use active larvae (active larvae have green droppings, there- of insecticide. Ladybird larvae and adults appeared to be no leaflets; (ii) branch hollows filled - more predatory at night, however, in low numbers they ices at the base of trunks during the day. Up to 200 lar- are not voracious enough to regulate the vast popula- after dark brown);2 (iii) presence of larval roosts in crev vae per 10 cm can be found under any adjacent stones, tions of E. discordis branches, old clothes, plastic rubbish, or anything dry of Ceraeochrysa sp. and Chrysoperla aff. externa (Chrys- and dark near the base of the trunk (Fig. 14). opidae) are also effective.larvae. InThese Ica and species Lambayeque, were observed larvae 3. Physical and biological control of Melipotis to consume a succession of E. discordis larvae, grasping Several methods of physical control of Melipotis were wrinkled orange remains. Chrysopidae species do have tried successfully in cultivated Prosopis groves or ‘hua- potentialwith mouthparts as biocontrol and sucking agents out of internalE. discordis fluids, larvae–as leaving rangales’ (see Fig. 14). The most practical method is to physically remove larvae from diurnal roosts, and feed et al. 2001). Some native species might be appropriate them to hens, which eat them voraciously. Roost traps they do for other plagues in the neotropics. 1994). (Albuquerque were created by placing or tying material–such as sack cloth–around the trunk or placing small wooden boards for Themass recording breeding of(Albuquerque E. discordis beinget al predated by rap- at the base of the trunk. Both serve to attract the entire idly moving wasp species, was more challenging. How- Melipotis larvae tree population during the day. Over a ever, both Polistes aff. peruvianus (Fig. 15c, d) and Pacho- few nights all larvae can be removed, thus arresting tree dynerus peruensis (Fig. 15e), were observed in Chiclayo defoliation and mortality. Biological control wasps were feeding on E. discordis observed, most commonly Polistes peruvianus (Hyme- parasitoid wasps were also found searching infected as well as large para- Prosopis larvae. SeveralE. unidentified discordis. small sitoid wasps. The endemic black-necked woodpecker leaflets and may also attack noptera:(Colaptes Vespidae),atricollis) was also observedunidentified excavating root species showed biological potential, including: the insid- roosts and eating larvae (Pecho et al. 2010). In laboratory Oriusconditions insidiosus in Lambayeque,) and a Reduviidae several bug. other

ious flower bug (

Table 1. Which defoliator? comparing Melipotis aff. indomita and Enallodiplosis discordis ap- pearance in Prosopis tree host.

Melipotisaff. indomita Enallodiplosis discordis

Appearance in Prosopis trees

deposits of larvae droppings deposits of dead yellow Trunk (2–3 mm) in bark crevices leaflets on bark & in crevices leaflets remain green & half eaten, remaining leaflets whole, with pale Leaves later no leaflets with rachis remaining circular blotches, or half yellow or yellow presence of larval roosts build-up of leaf-litter Trunk base during day, little leaf-litter 10–30 cm deep in sheltered positions progressively sparse, remaining yellow appearance, aging Canopy green leaflets, until defoliated leaf cohorts falling until tree defoliated

Insect appearance

first instar larvae hidden in new larvae small (<1.5 mm) pale orange Day leaves (<1.5 cm); then mature brown lozenge shape, stationary on leaflets. larvae (2.5–3.5 cm) found in roosts Third instar larvae mobile before pupation drop.

moth flies to take Prosopis flower first / second instar not visibly mobile. nectar and find mate. Night Third instar mobile, dropping into leaf-litter Brown larvae emerge from roosts to make loose cocoon and pupate. - columns up trunk, returning at dawn.

Rev. peru. biol. 27(4): 451 - 482 (November 2020) 475 Whaley et al.

plants including: Baccharis salicifolia, Encelia canescens, Grabowskia boerhaaviifolia, Lycium americanum, Phy- la canescens, Pluchea chingoyo, Trixis cacalioides and Waltheria ovata. These plant assemblages produce

2010a, 2019). The lack of any evidence of widespread bi- ologicalnectar-rich regulation flowers of throughout E. discordis the plague year to (Whaley date in Peru, et al. is likely to be a result of degradation including non-tar- geted destruction of biocontrol species and habitat. 5. The role of livestock in regulation ofEnallodiplosis discordis In protected areas, livestock can threaten natural re- generation, and so exclusion is attempted, as in ‘Santu- - land Prosopis arioto endemic Histórico species Bosque (see de Angulo Pómac’ & (a Sánchez sole protected 2016)). lowThe santuario is presently-dominated in a forest serious in ecological Lambayeque, upheaval, home with widespread Prosopis die-back and proliferation of post-rainfall climbers (Luffa operculata and non-native Momordica charantia) (pers. obs. and drone-mounted spectral analysis under permit). Recently, serious con-

Insecticide usage in Peru 1995 - 2013 (h) 5,000 - flicts and forest fires have ensued (see Radio Programas 4,000 mayo-juniodel Peru [RPP] 2018), https://rpp.pe/noticias/bosque-de-pom and are indicative of forest die-back. 3,000 ac); Pómac: Boletín de Santuario Historico de PomacProsop N°6,- 2,000 is forest (see above), the relationship between domestic 1,000 Given the regulatory mechanism of livestock in Tonnes of active ingredient Tonnes livestock and E. discordis 0 5 6 7 8 9 0 1 2 3 4 5 6 7 8 9 0 1 2 3 urgent research. 9 9 9 9 9 0 0 0 0 0 0 0 0 0 0 1 1 1 1 9 9 9 9 9 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 2 2 2 2 2 2 2 2 2 2 2 2 2 2 plague regulation here requires Year forest monitoring it emerged that (Source: UN FAO Statistics Division - Prosopis official data reported on FAO questionnaires from Peru) mature trees with livestock corralled below, maintained foliage,During whilst similar aged trees outside corrals, lost fo- Figure 15. Native insects observed as potential biological control liage and underwent die-back. In the corral, goats and agents of E. discordis. (a, b) Coccinellid ladybird larvae (cf. Cycloneda sheep consumed the Prosopis leaf-litter, whilst compact- sp. & Chilocorus sp.); (c, d) The once ubiquitous coastal wasp Polistes ing and soaking the ground with urine. peruvianus (Vespidae), also a voracious predator of Melipotislarvae; (e) The potter wasp Pachodynerus peruensis (Vespidae) seen con- This saw interruption of the E. discordis life cycle by suming E. discordis larvae; (f, g) Paraneda pallidula (Coccinellidae) killing larvae at the leaf-litter pupation stage, permitting typical of Peruvian Prosopis species; (h) Insecticide consumption in leaves to persist not subjected to defoliation cycles. Thus, Peru following the 1998–99 ENSO event (FAO) with unquantified Prosopis trees in traditional stock corrals were able to re- impact on native biocontrol insect populations. [Images © O. Whaley] tain canopy foliage and produce limited pods, compared with non-corralled trees or those with corralled cattle that did not. Although overgrazing with goats can accelerate de- Two introduced species–already recognised as bi- - ological control agents–also show potential to control tain densities and forest states, can also be important E. discordis Prosopissertification, seed in dispersers Piura research in dry revealed forest (Perevolotsky goats in cer are: the Clavicipitaceae fungus Isaria fumosorosea (Pae- cilomyces fumosoroseusat the pupation) and stagethe nematode on the ground; worm genusthese - Heterorhabditis. 1990,placed 1991,herbivores López (see 2017) Holmgren especially et followingal. 2006), Elin Niñothis rains.case, theGoats native (and seedsheep) dispersers to limited such extents, as white-tailedreplace dis Lastly, we observed small insectivorous birds feeding deer (Odocoileus virginianus) and desert fox (Lycalopex on E. discordis larvae, including the house wren (Trog- sechurae and L. culpaeus) (Huey 1969, Meza 2004) - deer lodytes aedon Xenospingus being hunted out and desert fox widely persecuted. This concolor). Unpublished research carried out in 2008 on being the case, livestock (at low density) may perform a an organic farm) and in the the lower slender-billed Ica valley, finch suggests ( that bio- vital role to help sustain forest health by consuming sur- control of E. discordis plague is possible in high diversi- face Prosopis leaf-litter, they regulate of E. discordis in the ty habitats. Here, where Prosopis-associated plants are ecosystem - as in the corral. cultivated for honey production, we recorded a higher concentration of the biocontrol species in understory

476 Rev. peru. biol. 27(4): 451 - 482 (Noviembre 2020) Ecología y diagnóstico de Enallodiplosis discordis (Diptera: Cecidomyiidae): un feroz defoliador de Prosopis

10 4 - 0 – 50

0 – 80 8 2 80 – 0 1 0

- 0 ( - )

5 20–0 5 – 3 can flush green with spring growth, then yellow

Figure 16. Leaf Cover Index (LCI) used as indicator of infection intensity and defoliation of Prosopis trees.

Today the number of goats and sheep in Peru is ap- times per month for three months, with around 1–4 kg of leaf-litter per clearance. After two weeks, tree canopies to 2012), whilst numbers of cattle are on the increase began to recover some foliage. Although producing very parently in significant decline (by nearly 59% from 1961 Forpus coeles- communities cite many factors contributing to the decline tis), after two years, trees treated in this fashion, had re- of(rising forest-run by 39% goats from and 1961 sheep, to not2012) least (INEI being 2012). the loss Rural of tainedfew pods foliage (consumed whilst untreated by Pacific trees parrotlets, died back. Prosopis pod forage as outlined. Other factors include: Clearly, the interruption of the lifecycle through market decline, community land tenure problems with as- physical removal of E. discordis pupae in the leaf-litter, sociated violence and insecurity, agroindustrial expansion does not prevent reinfection from adults travelling in blocking itinerant herder access, land abandonment due from other trees, but it does appear to maintain low- to drought, urban development, and migration. er levels of E. discordis reinfection from below the tree, To give an indication of this relationship, we conducted enabling the tree to outgrow infestation. Leaf-litter re- several small trials by physically removing leaf-litter un- moval is realistically only achievable with Prosopis trees der Prosopis E. near smallholdings. Further trials of physical interven- discordis, - Prosopis, at least near dwell- ter (5–10 cm (maturedeep, weighing trees c.90 around cm GBH) 20-25 infested kg) was with swept ings, to produce seed and survive. Likewise, it might be into a pile,in sprayed Ica and with Lambayeque. water and The composted sub-canopy under leaf-lit plas- antions appropriate are required strategy to allow to save some veteran (patrimo- nial) Prosopis trees. However, caution must be taken as tic to kill pupae. Subsequent leaf falls were cleared 1–2 Rev. peru. biol. 27(4): 451 - 482 (November 2020) 477 Whaley et al. the leaf-litter will play a role in conserving moisture Literature cited and insulating the roots from overheating. Here limited - irrigation might compensate for this, but again further - Adams AS,les Aylward colonising FO, Adams,historical SM, and Erbilgin naive N,host Aukema trees BH,are Cuas- In summary: rriesociated CR, Suenwith G,a bacterialRaffa KF. community2013. Mountain highly pine enriched beet research is required. in genes contributing to terpene metabolism. Applied – Prosopis trees are less susceptible to E. discordis in the following conditions: and Environmental Microbiology 79(11):3468–3475. http://dx.doi.org/ 10.1128/AEM.00068-13 – - - ter is consumed. Likewise, trees growing in cat- Albuquerqueraeochrysa GS, Tauber spp.: CA,potential Tauber for MJ, biological McEwen control PK, New in TR,the tleGrowing corrals, inside where livestock leaf-litter corrals is eaten where more leaf-lit out Whittington AE. 2001. Chrysoperla externa and Ce of desperation, but where urination impedes or kills the larva on the ground. New World tropics and subtropics, in: P.K. McEwen, T.Cambridge, R. New and pp. A.E. 408-423. Whittington https://doi.org/10.1017/ (Eds.), Lacewings in – Cultivated in the domestic or urban setting of theCBO9780511666117 Crop Environment. Cambridge University Press: garages, villages or next to dwellings, where the ground surface is hard, compacted or reg- externa (Neuroptera: Chrysopidae): life history and ularly swept. Albuquerquepotential GS, Tauberfor biological CA, Tauber control MJ. in 1994.Central Chrysoperla and South America. Biological Control 4(1):8–13. https://doi. – On sand dune slopes at valley margins or oases - org/10.1006/bcon.1994.1002 the sand slips away removing and burying pupae. - lling insects in a fragmented forest: incidence of ha- Altamiranobitat A, loss, Valladares edge effects G, Kuzmanich and plant N, availability. Salvo A. 2016. Journal Ga NotesTrees on Enallodiplosis here may also benefitdiscordis from as fogcontrol capture. agent of Insect Conservation 20(1):119–127. https://doi. for Prosopis org/10.1007/s10841-016-9845-2 Several Neotropical Prosopis species have been in- - troduced worldwide, especially P. juliflora and P. pallida Angulo F,de Sánchez Ornitólogos E. 2016. del Las Perú aves (UNOP), del Santuario 11(1), Históricopp.39-53. Bos que de Pómac, Lambayeque, Perú. Boletín de la Unión and Australia especially, introductions cause varying de- Bachman S, Moat J, Hill AW, de la Torre J, Scott B. 2011. Suppor- (often misidentified). In Hawaii, northern India, Ethiopia - to biodiversity, whilst often providing useful livelihood tial conservation assessment tool. ZooKeys 150:117– grees of impact; being highly invasive and detrimental ting126. Red https://doi.org/10.3897/zookeys.150.2109 List threat assessments with GeoCAT: geospa - linresources 2010). (e.g.In the Dahl future, 1971, Sosebee 1973, could DeLoach be considered 1985, - E. discordis Baena S, geMoat for plantJ, Whaley conservation. O, Boyd DS. PLoS 2017. One Identifying 12(11):e0188714. species asCordo a possible 1987, Moran agent with1993, which McKay to 2007, moderate Gallaher non-native & Mer https://doi.org/10.1371/journal.pone.0188714from the air: UAVs and the very high resolution challen Prosopis invasion. We would strongly advise against this for several reasons, but especially, as this insect has al- ready been found on at least six Prosopis tree species, Bale JS, Masterschange research: GJ, Hodkinson direct ID,effects Awmack of rising C, Bezemer temperature TM, and is unlikely to be selective, making old world Prosopis Brown VK et al. 2002. Herbivory in global climate vulnerable. Furthermore, in a new world order of climate https://doi.org/10.1046/j.1365-2486.2002.00451.x - on insect herbivores. Global Change Biology 8:1–16. troduced Prosopis, could allow the production of valuable 2009. The role of Prosopis in ecological and landsca- localchange, resources, pandemics and and over poverty; the long good term, management may even assist of in Beresford-Jones DG, Torres SA, Whaley OQ, Chepstow–Lusty AJ. ecosystems, particularly in irreversibly degraded arid coast Peru from the early horizon to the late interme- pe change in the Samaca basin, lower Ica Valley, south https://doi.org/10.1017/S1045663500002650Pu 1999, Felker & Moss 1996, Logan 2007, Shackleton et al. diate period. Latin American Antiquity 20(2):303–332. environments2014). Lastly, Prosopis needing species renewable from resources Peru introduced (see Garg to 2011. Two millennia of changes in human ecology: other countries (see Konda Reddy 1978), may one day be Beresford-Jonesarchaeobotanical DG, Whaley and OQ,invertebrate Alarcón C,records Cadwallader from the L. - tory and Archaeobotany 20:273–292. https://doi. requiredProsopis to restoresurvival forest and futureand culture Research back to Peru. lowerorg/10.1007/s00334-011-0292-4 Ica Valley, south coast Peru. Vegetation His Some Prosopis individuals (and groups or hybrid - swarms) appear to have genetic traits conferring a degree ca. Oxford University Press: Oxford. Beresford-Jones DG. 2011. Lost Woodlands of the Ancient Nas of resistance to E. discordis Boone CK, Keefover–Ring K, Mapes AC, Adams AS, Bohlmann Prosopis - J, Raffa KF. 2013. Bacteria associated with a tree–ki- vey research is needed to: plague.(i) identify Across genetically the Pacific resistant coastal lling insect reduce concentrations of plant defense clusters /distribution habitat, (ii) in identify Peru, further seed sources, UAV and (iii) ground recognize sur 1006. https://doi.org/10.1007/s10886-013-0313-0 compounds. Journal of Chemical Ecology 39(7):1003– areas for Prosopis events,niche requirements and (v) research of biological the Achilles control heel agents, of E. discordis (iv) locate–its 2015. Host range expansion of native insects to exotic dependence on leaf-litter soil seed for bank pupation. restoration prior to flood Branco M,trees Brockerhoff increases EG, with Castagneyrol area of introduction B, Orazio and C, Jactelthe pre H.- sence of congeneric native trees. Journal of Applied

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Whaley OQ,– Un Orellana recurso A, para Pérez su E, restauración Tenorio M, Quinteros y conservación. F, Mendo Ro- 2014. Prosopis: a global assessment of the biogeogra- za M, Pecho O. 2010a. Plantas y Vegetación de Ica, Perú Shackleton RT, Le Maitre DC, Pasiecznik NM, Richardson DM. world's worst woody invasive plant taxa. AoB Plants yal Botanic Gardens, Kew, UK. phy,6:plu027. benefits, https://doi.org/10.1093/aobpla/plu027 impacts and management of one of the nitrate) industry. Indian Journal of Chemical Techno- Wisniak J,logy Garces 8:427–438. I. 2001. The rise and fall of the salitre (sodium ecosystems. National Committee for the International Zachariades C, Hoffmann JH, Roberts AP. 2011. Biological con- Simpson BiologicalBB. 1977. Programme, Mesquite, its USA. biology in two desert shrub

trolhttps://doi.org/10.4001/003.019.0230 of mesquite (Prosopis species) (Fabaceae) in Cecidomyiidae) in the main biogeographical regions South Africa. African Entomology 19(2):402–415. Skuhraváof M. the 2005. world. Species Acta richnessSocietatis of Zoologicae gall midges Bohemicae (Diptera: 69:277–320. - ce for long‐distance, chemical gall induction by an Sopow SL, Shorthouse JD, Strong W, Quiring DT. 2003. Eviden org/10.1046/j.1461-0248.2003.00410.x insect. Ecology Letters 6(2):102–105. https://doi. Agradecimientos / Acknowledgments: - We would like to thank the staff of the following herbaria: K, USM, te control with Tordon 225 Mixture. Journal of Range UMOL, SGO, SI, CTES in UK, Chile and Argentina. This work would Sosebee RE,Management Dahl BE, Goen26:369–371. JP. 1973. Factors affecting mesqui not have been possible without the cooperation and support of the following institutions in Peru: Universidad Nacional Mayor de Sudzuki F. 1985. Utilización de la humedad ambiental por Pro- San Marcos, National Agrarian University – La Molina, Servicio Forestal y de Fauna Silvestre del Perú (SERFOR), Servicio Nacional - de Áreas Naturales Protegidas por el Estado (SERNANP), many tual del conocimiento sobre Prosopis tamarugo, Uni- rural communities in Ica, La Libertad, Piura and Lambayeque sopisversidad tamarugo de Tarapacá, Phil., in:Corporación M.A. Habit Nacional (Ed.), Estado Forestal, ac especially those of Comunidad Campesina San Francisco de Asís FAO, pp. 35–50. de Salas, and in Ica Huarangal, San Pedro, Usaca, Copara. In Peru, we thank the unfailing support of Claudia Luthi, and always feel Takahashi K. 2004. The atmospheric circulation associated her presence through the sunbeams of forest shade, also Alfonso Orellana and Alberto Benavides for their indefatigable support, with extreme rainfall events in Piura, Peru, during the along with Mario Tenorio, Evelyn Pérez and Octavio Pecho, as well - as Joaquín Leguía, Herbert Eichenlaub, Manuel Gonzales Barbadi- sicae 22 (11):3917–3926. https://doi.org/10.5194/ llo, Adriana Von Hagen, Gaston Cruz, Nora Grados, Carlos Reynel, 1997–1998angeo-22-3917-2004 and 2002 El Niño events. Annales Geophy Pascuala Juárez, Gualberto Gonzáles Ana Juárez, and particularly Alberto Esquen amongst many others. In the UK: David Beresford- - Jones, University of Cambridge; Tom Gregory (Previously at K), Institute of Archaeology, University College London. At Kew, the te change on insect invasions in temperate forest huge support from Gwlym Lewis, and so many including Terry Tobin PC, Parry D, Aukema BH. 2014. The influence of clima- Pennington, Lulu Rico Arce, Daniella Zappi, Bryn Dentinger, portunities for the World’s Forests in the 21st Cen- Chrissie Prychid, William Milliken, Amanda Cooper and Susana ecosystems, in: T. Fenning (Ed.), Challenges and Op Baena. We thank Vanessa Sutcliffe and Paulina Hechenleitner for their excellent editing and proofreading review. We would like to org/10.1007/978-94-007-7076-8_12 thank Michael Gates, Systematic Entomology Laboratory, Wash- tury; Springer: Netherlands, pp. 267–293. https://doi. ington, DC, and Samantha Gallagher, Alexandria, Virginia, for the - SEM photos of larvae. Michael Althaus, Silver Spring, Maryland, for the final arrangement and labelling of Plates 1–3. Finally, we Ueckert DN.2,4,5–T 1974. in Influence west Texas. of defoliation Journal of byRange the cutwormManagement Me would especially like to thank Bernard Verdcourt at Kew, for his lipotis27:153-155. indomita on control of honey mesquite with unique wisdom and guidance in the realm of insects, snails, fine coffee and much more.

2009. Prosopis species (Leguminosae), in: R. Mu- Conflicto de intereses / Competing interests: Van Klinken RD, Hoffmann JH, Zimmermann HG, Roberts AP. The authors declare that they have not incurred in conflicts of of Tropical Weeds using Arthropods, Cambridge Uni- interest. niappan,versity Press: G.V.P. New Reddy York, and USA, A. Raman, pp. 353–377. Biological Control Rol de los autores / Authors Roles: - OW: conceived, wrote and conducted fieldwork leading research; CB: supported fieldwork and physical control studies; OW, JM, RG: revised the manuscript; AB: contributed to research in biological Vargas H,Tamarugo Bobadilla (ProsopisD, Oyarzún tamarugo) M, Ramírez y Algarrobo O. 1989. Guía (Prosopis de re control in laboratory; TW, JM: data processing, niche modelling conocimientospp.). Instituto de de insectos Agronomía y otras de la especies Universidad que atacande Ta- and mapping; RG: provided essential guidance, taxonomy and rapacá, Corporación Nacional Forestal (CONAF). descriptions of larvae. Fuentes de financiamiento / Funding: 1977. Annotated checklist of the new world insects as- This work was not funded specifically, but was facilitated through Ward CR, O’Brien CW, O’Brien LB, Foster DE, Huddleston EW. funding and support from UK Darwin Initiative, legacies Royal Botanic Gardens, Kew; Sainsbury’s, UK; Seatrade, Barfoots UK.

sociated1557. 115pp. with the Prosopis (mesquite). United States Aspectos éticos / legales; Ethics / legals: Department of Agriculture Research Service Bulletin The authors declare that they have not incurred in unethical aspects. A, Leguía J. 2010b. An ecosystem approach to res- Whaley OQ,toration Beresford-Jones and sustainable DG, Milliken management W, Orellana of dry forestA, Smyk in Southern Peru. Kew Bulletin 65:613–641. https://doi. org/10.1007/s12225-010-9235-y

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