Androthrips ramachandrai Karny is an exotic thrips, assumed to be predacious, and is associated with gall-inducing thrips. It was first reported in the U.S. from FL, and intercepted in CA from Thailand in 2002. We surveyed Ficus spp. with Gynaikothrips-induced galls in AL, CA, FL, HI, LA, MS, and TX, and document that A. ramachandrai is now established in CA, FL, HI, and TX. It probably has been spread by the ornamental horticulture industry. We outline its biology and compare it to a congener A. flavipes, a documented thrips predator. Androthrips ramachandrai has the potential to be a beneficial biological control agent and a hindrance to weed biological control.
Held et al. (2005) predicted that gall-inhabiting arthropods found in Gynaikothrips-induced galls on Ficus spp. could be inadvertently transported within the continental U.S. through the ornamental plant industry. Androthrips ramachandrai Karny (Thysanoptera: Phlaeothripidae) is known to inhabit the galls of both Gynaikothrips uzeli (Zimmermann) and G. ficorum (Marchal) (Thysanoptera: Phlaeothripidae) (Takahashi 1934), and is probably being moved throughout the U.S. in shipments of nursery-grown Ficus.
The first record of A. ramachandrai in the U.S. was of two specimens collected in March 2002, Miami-Dade Co., FL from Ficus microcarpa (Moraceae) galled by G. ficorum (Nakahara & Edwards 2002). Another collection of A. ramachandrai was made from Riverside Co., CA on 02 Aug of the same year (Gaimari 2005). It was intercepted during a federal foreign-quarantine inspection along with Gigantothrips elegans Zimmermann (Thysanoptera: Phlaeothripidae) and Gynaikothrips malabaricus Ramakrishna on Ficus sp. imported from Nong Nooch Tropical Botanical Garden in Thailand (G. Watson, California Department of Food and Agriculture, pers. comm.).
Androthrips ramachandrai was described from India and found in association with the gall thrips Austrothrips cochinchinensis Karny (Thysanoptera: Phlaeothirpidae) on Calycopteris (=Getonia) floribunda (Combretaceae) (Karny 1926). Worldwide, Androthrips contains 12 species (Mound 2005). Androthrips flavipes Schmutz is a known predator of thrips (Ananthakrishnan & Varadarasan 1977; Varadarasan & Ananthakrishnan 1981), and other Androthrips species are assumed to be predators, too, but little or nothing is known about their biology.
Androthrips ramachandrai (Fig. 1) is dark brown to black. It can be distinguished from other dark, large phlaeothripids by its large fore femora with a strong, cylindrical tooth near the base followed by a row of small tubercles (Fig. 2). Its tube (abdominal segment X) is almost half the length of Gynaikothrips spp., which is easily detectable. It can be separated from other Androthrips by the dark middle and hind tibiae (Karny 1926).
Not much is known about the biology of A. ramachandrai. It is rare in newly formed galls of Austrothrips cochinchinensis. However, as galls mature, A. ramachandrai becomes more abundant as the population of A. cochinchinensis declines (Ananthakrishnan 1978), which might indicate that A. ramachandrai is predacious on the gall-inducing thrips, similar to A. flavipes (Ananthakrishnan & Varadarasan 1977).
Currently, A. ramachandrai is known from Australia, Costa Rica (L. Mound, pers. comm.), India (Karny 1926), Taiwan (Takahashi 1934), and Thailand (Ananthakrishnan 1978). Herein we report its establishment in the U.S.
The purpose of this paper is to document the currently known distribution of A. ramachandrai in the U.S., provide a brief overview from the literature of its biology, and increase the awareness of regulatory and research entomologists in North American to this thrips, which could become economically and ecologically important.
Materials and Methods
We collected and solicited Gynaikothrips-induced galls from the following states in the U.S.: AL, CA, FL, HI, LA, MS, and TX. Galls and contents were collected in the field, preserved immediately in 95% ethanol, and taken to the lab for identification of the thrips. Museum records were requested for A. ramachandrai from CA (California Department of Agriculture), FL (Florida State Collection of Arthropods), and TX (Texas A & M University).
Results and Discussion
Ficus galls collected from South Padre Island, Cameron Co., TX by DWH on 24 Aug 2005, from Riverside Co, CA by Chris Hanlon (University of California, Riverside) on 08 Mar 2005, and from Oahu Island, HI by Frank Howarth (Bishop Museum, Honolulu) on 17 Apr 2006 contained specimens of A. ramachandrai. Galls from TX were initiated by G. uzeli and collected from 7 Ficus trees at 2 locations (Table 1). Galls from CA were initiated by G. ficorum and collected at 1 location with a total of 258 G. ficorum and 21 A. ramachandrai (total number of galls not known). Galls from HI were initiated by G. ficorum and collected at 1 location with 16 G. uzeli. Voucher specimens of G. ficorum, G. uzeli, and A. ramachandrai from CA and TX have been deposited in the USDA, ARS, Systematic Entomology Laboratory, Beltsville, MD; and A. ramachandrai from HI have been deposited in the Bishop Museum, Honolulu, HI.
The Florida Department of Plant Industry has at least 44 records of A. ramachandrai (2002-2006) from 11 southern counties in Florida (Brevard, Broward, Miami-Dade, Glades, Hillsborough, Lee, Martin, Monroe, Palm Beach, Pinellas, and Sarasota) and from the following plants: Artocarpus heterophyllus (Moraceae); Ficus benjamina and F. microcarpa (Moraceae); Malvaviscus penduliflorus (Malvaceae); Schefflera actinophylla (Araliaceae); and Tabebuia heterophylla (Bignoniaceae).
The California Department of Food and Agriculture has one record of A. ramachandrai collected from F. microcarpa originating from Irvine Co. and intercepted in Santa Clara Co. on 09 Nov 2004. Galls collected or solicited from AL, LA, and MS did not contain specimens of A. ramachandrai, and no further museum records were available for TX.
The 2 records from California are new state records, because the previous record was an intercepted specimen from Thailand (see above). The records from Texas and Hawaii also are new state records.
Our findings from TX (Table 1) might indicate that Gynaikothrips populations decline during an increased presence of A. ramachandrai. However, further data is needed to substantiate this claim. The trend is consistent with a pattern found by Anathakrishnan (1978) in which populations of Austrothrips cochinchinensis decreased as A. ramachandrai progressively increased.
Montandoniola moraguesi (Puton) (Hemiptera: Anthocoridae) was present in the galls from TX and HI. This anthocorid is known to feed on gall-inducing thrips and also on A. ramachandrai and A. flavipes (Dobbs & Boyd 2006). What impact this anthocorid might have on the effectiveness of A. ramachandrai in reducing pest thrips populations is not known. Another natural enemy of Gynaikothrips is the wasp Thripastichus gentilei (del Guercio) (Hymenoptera: Eulophidae), which parasitizes species of Androthrips (Loomans et al. 1997). What quantitative impact these 3 natural enemies (individually or together) have on pest-thrips populations and on each other remains unassessed.
Nothing is known about the ecology of A. ramachandrai, but some information may be inferred from the better-studied congener A. flavipes. When adults of A. flavipes enter mature galls of Arrhenothrips ramakrishnae Hood (Thysanoptera: Phlaeothripidae), they feed on about 10% of the available prey and deposit eggs in galls near their prey eggs. After hatching, the larvae consume most of the remaining prey and resort to cannibalism. This behavior can occur whether prey is abundant or not and is a limiting factor to its own population growth (Varadarasan & Ananthakrishnan 1981). Typically they feed on the eggs and larvae, but not adults. By the time the larvae pupate, they have devoured almost 80% of available prey (Sureshkumar & Ananthakrishnan 1987). Androthrips flavipes develops faster than the galling thrips, which enables the predator to complete its life cycle more quickly than the prey (Varadarasan & Ananthakrishnan 1982). Strangely, the enlarged fore femora of adult A. flavipes are not used in subduing prey (Varadarasan & Ananthakrishnan 1982; Sureshkumar & Ananthakrishnan 1987).
Because A. ramachandrai feeds primarily on the immature stages of thrips in galls, this does not preclude it from attacking the immature stages of surface feeding thrips. In a laboratory trial, A. flavipes readily consumed thrips prey in a Petri dish (Varadarasan & Ananthakrishnan 1981). In FL, where A. ramachandrai is well established, there may be possible biotic interference (Reimer 1988) with thrips, particularly phlaeothripids such as Pseudophilothrips ichini (Hood) (Thysanoptera: Phlaeothripidae), used for biological control of invasive peppertrees (Cuda et al. 2005). The effectiveness of the weed biocontrol Liothrips urichi Karny (Thysanoptera: Phlaeothripidae) released for biocontrol of the weed, Clidemia hirta (Melastomataceae), in HI has been reduced by generalist predators (Reimer 1988).
Androthrips ramachandrai is now established in 3 continental U.S. states and HI, but very little is known about its biology or ecology. It is assumed to be predacious and could potentially have an impact on thrips populations, including pests and weed biological control agents. Its presence could cause biotic interference (Reimer 1988) or it could prove to be a successful natural enemy against Gynaikothrips spp. on ornamental Ficus. We intend this information to increase the awareness of regulatory agents and facilitate the identification of this potentially important thrips.
Acknowledgments
We thank C. Hanlon (University of California, Riverside), Frank Howarth (Bishop Museum, Honolulu, HI), and R. Messing (University of Hawaii, Kapaa) for providing material from their respective locations. We thank G. B. Edwards (Florida Department of Agriculture and Consumer Services) for providing records of A. ramachandrai in Florida. We thank E. G. Riley (Texas A&M), G. Watson (California Department of Food and Agriculture), and D. Nickle (USDA, ARS, SEL) for checking their respective collections for specimens of A. ramachandrai. We thank L. Mound (CSIRO Entomology, Canberra, Australia), B. Sampson (Mississippi State University), and two anonymous reviewers for providing helpful comments to an earlier draft of the manuscript. We gratefully acknowledge G. Watson for providing Fig. 1A.
References Cited
Fig. 1.
Dorsal view of Androthrips ramachandrai from Riverside Co., CA. (A) Slide mounted, cleared specimen and (B) wet mounted specimen. Scale bar = 1 mm.
Fig. 2.
Fore femur of Androthrips ramachandrai from Riverside Co., CA. (A) Wet mounted, right ventral fore femur and (B) slide mounted, cleared left fore femur. The white arrow is pointing to the strong, cylindrical tooth near the base and back arrow to the row of small tubercles. Scale bars = 250 μm.
