University of California, Riverside

Applied Biological Control Research



Final Report on Cottony Cushion Scale


Final Report on the Classical Biological Control of Cottony Cushion Scale (el Pulgon) with Rodolia cardinalis (la Mariquita) in the Galápagos Islands

Mark S. Hoddle1,2, Christina D. Hoddle1, Roy G. Van Driesche3, and Charlotte Causton4

1Department of Entomology, University of California, Riverside CA 92521. Mark.hoddle@ucr.edu
2Center for Invasive Species Research, University of California, Riverside, CA 92521
3Department of Plant, Soil, and Insect Sciences, University of Massachusetts, Amherst, MA 01003. vandries@nre.umass.edu
4Charles Darwin Foundation, Puerto Ayora, Santa Cruz, Galápagos Islands. Charlotte.causton@fcdarwin.org.ec

Executive Summary: The cottony cushion scale, Icerya purchasi, a cosmopolitan sap sucking plant pest native to Australia was discovered in the Galápagos in 1982. It readily dispersed to at least 15 different islands in the Galápagos archipelago. High density populations retarded plant growth, and the excretion of sugary waste product, honey dew, provided a substrate for black sooty molds that grew on leaves and stems disfiguring plants. Honey dew is a rich carbohydrate source highly attractive to invasive ant species which tend Icerya colonies harvesting this waste product. Icerya has been recorded infesting 98 native or endemic plants, 17 of which are on the IUCN Red List of Threatened Species, of which a further five are classified as Endangered or Critically Endangered.

In 1996, the Charles Darwin Foundation and the Galápagos National Park Service formed a Technical Advisory Committee to address the Icerya invasion. The Committee concluded that mitigation with pesticides was infeasible, and that biological control with a predatory beetle, Rodolia cardinalis, offered the best prospect for permanent and widespread suppression of Icerya. In 1999, Rodolia was imported into Quarantine at the Charles Darwin Research Station to undergo rigorous safety testing to evaluate the threat this natural enemy would pose to non-target species, especially native or endemic insects. Analysis of quarantine studies coupled with the published studies on the use of Rodolia for Icerya control in numerous other countries led to the conclusion that this natural enemy would not present a significant threat to non-target species in the Galápagos.

In 2002, Rodolia was released onto 11 different islands, and rapid suppression (sometimes within ~3 months) of Icerya was observed. In October 2009, a two year evaluation project was initiated to assess the impact of Rodolia on Icerya across four different habitats on Santa Cruz and for a 12 month period on San Cristóbal.

The project had three major objectives:

    1. Survey islands for the presence of Icerya and Rodolia in urban, agricultural, and wilderness areas,
    2. Measure the degree of suppression of Icerya by Rodolia in the Galápagos, and
    3. Investigate under field-like conditions the hypothesis that Rodolia has a limited prey range as predicted by quarantine laboratory studies.

Results from this two year project indicate: (1) Rodolia is persisting on islands where it was originally released and has tracked Icerya to islands where it was not intentionally released. (2) Icerya populations are typically very low in most areas surveyed. Notable exceptions existed on certain host plants (especially Scaevola plumieri and Rhynchosia minima; or when honey-dew collecting ants were present and guarded Icerya from Rodolia [ant tending was most pronounced in urban areas on San Cristóbal]) (3) No evidence for non-target attacks was found from either field observations or behavioral experiments conducted in large walk-in cages that held potted plants infested with Icerya and a range of potential non-target prey species. It is concluded from these studies that Rodolia continues to provide high levels of control of Icerya on most host plants in the majority of affected ecosystems in the Galápagos, and that biocontrol is safe as no non-target impacts were observed.

rodolia eating iceyaOverview: Cottony cushion scale, Icerya purchasi Maskell (Hemiptera: Coccoidea: Monophlebidae: Iceryini), an exotic plant pest in the Gálapagos, has been the target of a classical biological control program with the predatory beetle, Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae). Host specificity testing in quarantine in the Galápagos indicated that R. cardinalis posed negligible threat to non-target species in the Galápagos and it exhibited high host specificity towards the intended target, I. purchasi. Rodolia was liberated in January 2002 in the Galápagos and it provided rapid control of Icerya in all areas (lowland arid, highland agricultural, and urban) and across most infested plant species (native and exotic) that suffered high pest densities prior to 2002. Seven years after the release of Rodolia, the biological control program against Icerya with this predator was considered mature enough to be evaluated vigorously for in terms of successful suppression of the target pest, Icerya, and for non-target impacts. In October 2009, a two year evaluation project for Icerya biological control was initiated. For three months (Oct. – Dec. 2009) survey and experimental work was conducted by M.S. Hoddle, C.D., Hoddle, and R.G. Van Driesche in cooperation with the Charles Darwin Research Foundation, the Galapagos National Park Service, and SICGAL. The project was maintained until November 2011 by a Charles Darwin Research Station volunteer, Claudio Crespo Ramírez, who conducted monthly field surveys for Icerya and Rodolia on native plants at selected study sites on Isla Santa Cruz. Field surveys were also conducted for 12 months (Dec. 2009 to Dec. 2010) at two sites on San Cristóbal, Cerro Colorado and Puerto Baquerizo, by José Loayza (SICGAL).

Research Objectives: The goals of this project were : (1) to survey islands for the presence of Icerya and Rodolia in urban, agricultural, and wilderness areas with either visual plant inspections (for Icerya and Rodolia) or through the use of yellow sticky traps hung in or near Icerya-infested hosts (for Rodolia), (2) to measure the degree of suppression of Icerya by Rodolia in the Galápagos, and (3) to investigate under field-like conditions the hypothesis that Rodolia has a limited prey range as predicted by quarantine laboratory studies.

Results:

Objective 1: Monitoring Islands for the Presence of Icerya and Rodolia.

Table 1. Distribution of R. cardinalis in 2002 and 2009
Islands where R. cardinalis was released in 2002 Islands where R. cardinalis was found in 2009
Santa Cruz Santa Cruz
San Cristobal San Cristobal
Floreana Floreana
Isabela Isabela
Santiago Not surveyed sufficiently
Fernandina Fernandina
Marchena Marchena
Pinta Not checked
Pinzon Not surveyed sufficiently
Rabida Not surveyed
Genovesa Not surveyed 
  Baltra
  Champion*
* New record in 2009 for I. purchasi and R. cardinalis

Islas Santa Cruza,b, Baltraa,b, Isabelaa,b, Floreanaa,b, San Cristóbala,b, Championa, Españolaa, Marchenab, and Fernadinaa,b were surveyed for the presence of Icerya and Rodolia via visual observations of native plants (a performed for Icerya and Rodolia) or with sticky traps hang in bushes and trees (b to capture Rodolia.) Icerya and Rodolia were found on all of the islands that were surveyed except Española. Icerya and Rodolia have not been reported previously from this island. Survey results are presented in Table 1. Rodolia cardinalis was observed or collected on sticky traps in a wide range of vegetation types, ranging from xeric habitats to upland humid and dry areas on the edges of volcanoes (altitude range of 0 to 1200 m elevation) as well as in urban areas, agricultural areas and areas of the National Park. Between 2002 and 2009, R. cardinalis occurred in 40 of 112 (36%) of known host plants I. purchasi (Table 2). Ten of these records are endemic species of plants including endangered species Darwiniothamnus tenuifolius, Calandrinia galapagosa and Scalesia cordata. Rodolia cardinalis was also found on 16 native species, including four species of native mangroves (Avicennia germinans, Conocarpus erectus, Laguncularia racemosa, and Rhizophora mangle), and 14 species of introduced plants (Calderon Alvarez et al., 2012).

 

Preparing sticky cards for surveys Deploying sticky cards Inspecting plants for Iceya rodolia
Preparing sticky cards for surveys Deploying sticky cards at field sites to capture Rodolia Inspecting plants for Icerya and Rodolia

 

Table 2 Known host plants of I. purchasi in Galapagos indicating species where R. cardinalis was recovered between 2002-2010 (from Calderón Alvarez et al. 2012) 

Family Species (Origin,IUCN status)

R. cardinalis present

Family Species (Orgin,IUCN status) R. cardinalis present
Acanthaceae Avicennia germinans (N) + Caesalpinaceae Bauhinia monandra (I) +
  Blechum pyramidatum (N)     Parkinsonia aculeata (N) +
Amaranthaceae Alternanthera echinocephala (N)     Senna obtusifolia (I)  
Anacardiaceae Mangifera indica (I) +   Senna occidentalis (N)  
Annonaceae Annona cherimola (I) +   Senna pistaciifolia (N) +
 Apiaceae Cyclospermum leptophyllum (N?)    Celastraceae Maytenus octogona (N)  
 Apocynaceae Nerium oleander (I)    Combretaceae Conocarpus erectus (N)  
  Vallesia glabra (N)     Laguncularia racemosa (N)  +
 Arecaceae Cocos nucifera (I)   Convolvulaceae Ipomoea habeliana (E, LC)  
Asteraceae  Brickellia diffusa (N)     Ipomoea nil (I)  
  Darwiniothamnus lancifolius (E, EN)     Ipomoea pes-caprae (N)  
  Darwiniothamnus tenuifolius(E, EN)  +   Merremia aegyptia (N)  
  Gamochaeta purpurea (N?)   Cyperaceae Cyperus anderssonii (E, LC)  
  Lecocarpus darwinii (E, EN)   Euphorbiaceae Acalypha abingdonii (E, VU)  
  Lecocarpus pinnatifidus (E, CR)     Acalypha parvula (E, LC)  
  Macraea laricifolia (E, LC)  +   Acalypha wigginsii (E, CR)  
  Porophyllum ruderale (I)     Chamaesyce amplexicaulis (E, LC)  
  Scalesia aspera (E, VU)     Chamaesyce punctulata (E, LC)  
  Scalesia atractyloides (E, CR)     Chamaesyce viminea (E, LC)  +
  Scalesia baurii (E, VU)     Croton scouleri (E, LC)
  Scalesia cordata (E, EN)  +   Euphorbia cyathophora (I)  
  Scalesia divisa (E, EN)     Phyllanthus acidus (I)  
  Scalesia gordilloi (E, CR)     Phyllanthus caroliniensis (N)   
  Scalesia helleri (E, VU)     Phyllanthus caroliniensis (N)   
  Scalesia helleri (E, VU)     Ricinus communis (I)  +
  Scalesia pedunculata (E)   Fabaceae Cajanus cajan (I)
 Bombacaceae Matisia cordata (I)     Canavalia maritima (N)  
 Boraginaceae Cordia leucophlyctis (E)     Centrolobium paraense (I)  
  Cordia lutea (N) +   Crotalaria incana (N)  
  Heliotropium angiospermum (N)      Desmanthus virgatus (N)  
  Tournefortia psilostachya (N)      Desmodium incanum (N?) +
  Tournefortia rufo-sericea (E, VU)     Phaseolus mollis (E, NT)  
Brassicaceae Brassica oleracea (I)     Phaseolus vulgaris(I)  
Burseraceae Bursera graveolens (N) +   Piscidia carthagenensis (N) +
Cactaceae Jasminocereus thouarsii (E, VU) +   Rhynchosia minima (N) +
Fabaceae  Stylosanthes sympodiales (N)   Nyctaginaceae Pisonia floribunda (E, LC)  
   Vigna luteola (N)  + Passifloraceae Passiflora quadrangularis (I)  +
 Goodeniaceae Scaevola plumieri (N)  + Plumbaginaceae Plumbago scandens (N)  
 Lamiaceae Hyptis pectinata (I)   Polygalaceae Polygala galapageia (E, VU)  
  Mentha piperita (I)   Portulacaceae Calandrinia galapagosa (E, CR)  +
  Ocimum basilicum (I)     Portulaca oleracea (N?)  +
 Malvaceae Bastardia viscosa (N)   Punicaceae Punica granatum (I)  
  Gossypium darwinii(E, LC)  + Rhizophoraceae Rhizophora mangle (N)  
   Gossypium klotzschianum (E, NT)    Rosaceae Rosa sp.(I)  
  Hibiscus rosa-sinensis (I) + Rubiaceae Borreria ericaefolia (E)  
  Hibiscus tiliaceus (N)     Chiococca alba (N)  
Mimosaceae Acacia insulae-iacobi (N)     Psychotria rufipes (E, VU)  
  Acacia macracantha (N) + Rutaceae Citrus aurantiifolia (I) +
  Acacia nilotica (I) +   Citrus sinensis (I) +
  Acacia rorudiana (E?) + Scrophulariaceae Russelia equisetiformis (I) +
  Inga edulis (I) +   Scoparia dulcis (N)  
  Neptunia plena (N)   Sterculiaceae Waltheria ovata (N) +
  Prosopis juliflora (N) + Ulmaceae Trema micrantha (N?)  
Moraceae Ficus sp. (I) + Verbenaceae Clerodendrum molle (E, VU) +
Myrtaceae Psidium guajava (I) +   Lantana camara (I)  
Nyctaginaceae Commicarpus tuberosus (N)     Lantana peduncularis (E, LC)  
  Cryptocarpus pyriformis (N)     Tectona grandis (I)  

a Key: Origin: E =Endemic, N = Native, I = Introduced; IUCN status: CR = critically endangered, EN = endangered, VU = vulnerable, NT = near threatened, LC = least concern; Species in bold = mortality attributed to I. purchasi

Objective 2: Measuring Suppression of Icerya Populations by Rodolia.

To determine the degree of suppression of Icerya populations by Rodolia on several major native plants in relatively undisturbed native habitats four study sites were selected on Santa Cruz: (1) El Barranco adjacent to the Charles Darwin Research Station (Photo A), (2) the paved pathway leading to Tortuga Beach, (3) stands of uva-del-mar in sand dunes behind Tortuga Beach (Photo B), and (4) white mangroves near the Playa Estación at the Charles Darwin Research Station (Photo C).

These sites were monitored monthly and numbers of Icerya and Rodolia from timed (1 min) searches of selected plants were recorded over a 2-yr period (Oct. 2009 – Nov. 2011). These count data provided information on the relative densities of Icerya and Rodolia on different host plants through time. Survey results suggest that overall Icerya populations were low over the 2-yr period surveys were conducted. For example, prior to the release of Rodolia, white mangroves were heavily infested with Icerya. Following the release of Rodolia, Icerya populations declined on white mangroves (Calderon et al., 2012). At the end of 2011 when surveys were terminated, Icerya populations remained very low on white mangroves over the 2-yr survey period at sites that were heavily infested prior to the commencement of the biocontrol program (Graph A).

El Barranco Survey Uva Del Mar Claudio sampling white mangroves
Surveying for Icerya in El Barranco.  Uva-del mar infested with Icerya at Tortuga Beach Claudio Crespo Ramírez sampling white mangroves at Playa Estación

 

Populations of Icerya and the percentage of plants infested in Puerto Baquerizo on San Cristóbal declined when Rodolia populations increased
Graph A (above). Monthly monitoring of Icerya populations on white mangroves at Playa Estación over a 2-yr period indicate that this pest was consistently maintained at very low levels (typically less than 1 adult Icerya per plant and less than 8% of sampled plants being infested.)

In some areas and on certain host plants, Icerya populations persisted at notably higher densities in comparison to other sites that were surveyed. The most notable of these sites was the Icerya infestation on uva-de-mar (Scaevola plumieri) at Tortuga Beach (Graph B). At this study site, Icerya was consistently present on uva-de-mar, but the percentage of infested plants increased and decreased over the 2-yr survey period. As pest densities increased, Rodolia populations rebounded and approximately 2-6 months later Icerya populations would decline again as predator populations peaked (Graph B). It is unknown why this phenomenon was so pronounced at Tortuga Beach. It could be due to the host plant (uva-de-mar may be a very good host for Icerya, but Rodolia struggles to search for prey on this plant) or the sand dune habitat (this location may be highly favorable for Icerya but less preferred by Rodolia.) The interactive effects of Icerya-Rodolia-Host-Plant-Location at this site would be ideally suited for perturbation experiments designed to tease out the underlying factors driving these observed population cycles.

Percentage of uva-de-mar at Tortuga Beach infested with adult Icerya and Rodolia over a 2-yr period suggest that the pest exhibits population increases and decreases which could be driven by Rodolia predation.
Graph B (above). Percentage of uva-de-mar at Tortuga Beach infested with adult Icerya and Rodolia over a 2-yr period suggest that the pest exhibits population increases and decreases which could be driven by Rodolia predation.

Icerya populations were monitored for 12 months on San Cristóbal at two different sites, an undisturbed natural area on Cerro Colorado dominated by Waltheria ovata and Rhynchosia minima, and a mixed variety of plants (e.g., citrus, guava, Waltheria and Rhynchosia) in a largely urbanized area, Puerto Baquerizo Moreno. Similar population trends were observed on San Cristóbal as Santa Cruz, when Rodolia populations increased on infested plants, Icerya numbers declined (Graph C).

Populations of Icerya and the percentage of plants infested in Puerto Baquerizo on San Cristóbal declined when Rodolia populations increased.
Graph C (above). Populations of Icerya and the percentage of plants infested in Puerto Baquerizo on San Cristóbal declined when Rodolia populations increased.

The presence of ants tending Icerya maybe disadvantageous for Rodolia. Field surveys on San Cristóbal indicated for both urban and wilderness areas, that ants were associated with high density populations of Icerya, and Rodolia presence was low or absent (Graph D).

Ants tending Icerya on Waltheria ovata and Rhynchosia minima on Cerro Colorado, San Cristóbal may be responsible for the low levels of activity by Rodolia on these infested plants.
Graph D (above). Ants tending Icerya on Waltheria ovata and Rhynchosia minima on Cerro Colorado, San Cristóbal may be responsible for the low levels of activity by Rodolia on these infested plants.
Icerya on an infested plant Icerya ant farm Black sooty mold substrate
High density ant populations tending Icerya on an infested plant in Puerto Baquerizo, San Cristóbal may aggressively exclude Rodolia from Icerya infestations Ants "farm" Icerya because this pest provides them with a sugary waste product, honeydew. This honeydew drips onto leaves providing a substrate for the growth of black sooty mold


Objective 3: Investigating the Prey-Range of Rodolia under Field-Like Conditions.

The feeding preferences and behavior of Rodolia were studied over Oct - December, 2009 in large cages at the Charles Darwin Research Station. The cages held native plants (e.g., Parkinsonia aculeata, Gossypium spp., Acacia macracantha, and Waltheria ovata) that were infested with Icerya (the target) and non target prey species (e.g., Coccus viridis, Ceroplastes, spp., mealybugs, aphids, and spider mites). Starved field collected and lab reared adult Rodolia were released into cages and their foraging behaviors and prey choices were recorded visually. More than 30 adult beetles were observed and almost 30 hours of visual observations were made. Rodolia was never observed attacking non-target species. All feeding and oviposition events occurred on the target, Icerya. These results and our field observations support previous quarantine findings that showed that Rodolia is an extreme specialist on Icerya and it is very unlikely to feed on other insects in the Galápagos.

Field Cages Rodolia larva searching for prey Rodolia larva attacks Icerya
Field cages used for behavioral observations Rodolia larva searching for prey Rodolia larva ignores Ceroplastes and attacks Icerya.

 

Outreach Efforts: Whenever possible efforts were made to provide information on the biological control of Icerya with Rodolia to interested people and organizations. Extension of information occurred in one of two ways: (1) informal discussions with people who expressed an interest in what was being done in the field. Discussion of this project under these conditions typically occurred on the Charles Darwin Research Station property, or in public areas around Tortuga Beach or in Puerto Ayora. (2) Formal outreach was achieved through two seminars that were given to the Galápagos National Park Service (Causton on October 5 2009, and Van Driesche December 11 2009), and via verbal updates presented to SICGAL (Mark and Christina Hoddle November 12, 2009 to David Arana).

Charlotte Causton Talk

Summary: Data collected over a 2-yr period (Oct. 2009 – Nov., 2011) suggest that: (1) the introduced predator Rodolia cardinalis has survived and spread since its initial introduction into the islands in 2002. It is now widely present in many areas and habitats, having colonized islands infested with Icerya without human assistance (i.e., self-introduced). (2) The pest has been suppressed to non damaging levels on many important native host plants, including white mangrove, Acacia species, Waltheria, Prosopis, Parkinsonia, but less so on uva-del-mar and Rhynchosia minima. These plants, especially white mangrove are ecologically important species that were heavily attacked by Icerya before the release of Rodolia. (3) In addition to being effective, the project has been safe. There is no evidence of attack by free-ranging Rodolia on non-target insects from more than 30 hrs of behavioral observations in large field cages where a range of alternative prey species were provided on potted native plants. All recorded predation events were solely on Icerya, the intended prey species of the biocontrol project. Further, during field surveys, no evidence of Rodolia attacking non-Icerya prey species was found. Even when non-target insect species were in close proximity to Icerya, Rodolia was always found feeding on the target pest.

Conclusion: From the results of 2 years of population monitoring of Icerya in several distinct habitats coupled with behavioral studies on the predation preferences of Rodolia, it is concluded that the biocontrol program has been very successful in two regards: (1) permanently suppressing damaging populations of the target pest, Icerya,on a wide variety of host plants in diverse habitats, and (2) safety, as no evidence for adverse non-target impacts has been found.

Inventories to determine the distribution of R. cardinalis should be continued. Besides this, it is recommended that the impact of the biological program on Darwiniothamnus and Scalesia species should be assessed to determine whether there is the same level of control of I. purchasi as found in this study.

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References Cited:

  • Calderón Alvarez, C.; Causton, C. E.; Hoddle, M. S.; Hoddle, C. D.; Driesche, R. van; Stanek, E. J., III (2012) Monitoring the effects of Rodolia cardinalis on Icerya purchasi populations on the Galápagos Islands. BioControl 57: 167-179.
  • Causton CE (2001) Dossier on Rodolia cardinalis Mulsant (Coccinellidae: Cocinellinae) a potential biological control agent for the cottony cushion scale Icerya purchasi Maskell (Margarodidae). Charles Darwin Foundation, Galapagos, Unpublished report

 

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