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Biological Control 29 (2004) 326–331

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Field assessment of a frond-feeding weevil, a successful


biological control agent of red waterfern, Azolla filiculoides,
in southern Africa
A.J. McConnachie,a,* M.P. Hill,b and M.J. Byrnea
a
Ecophysiological Studies Research Program, School of Animal, Plant and Environmental Sciences, University of the Witwatersrand,
Private Bag 3, Wits, 2050 Johannesburg, South Africa
b
Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown 6140, South Africa
Received 25 February 2003; accepted 25 August 2003

Abstract

Azolla filiculoides (red waterfern) is a small, floating fern native to South America, that has invaded aquatic habitats, pre-
dominantly water resevoirs in southern Africa. A frond-feeding weevil, Stenopelmus rufinasus Gyllenhal (Coleoptera: Curculioni-
dae), was imported from Florida, USA, and released as a biological control agent against this weed in South Africa at the end of
1997. To date, 24,700 weevils have been released, which has resulted in local extinction of red waterfern at 81% of the 112 release
sites. The weevil has not failed to control a single site. Several sites were, however, lost due to flooding or drainage of dams. The
surface area of weed controlled totalled 203.5 ha. On average, A. filiculoides was controlled in infested sites in 6.9 (4.3) months. The
weed recolonized at 22 of the sites (through either spore germination or dispersal by waterfowl), but the weevils subsequently spread
to all of these sites and successfully caused local extinction of the weed at 18 of the sites. Five years after the release of the weevil, the
weed no longer poses a threat to aquatic systems in southern Africa. In comparison to other biological control programs of aquatic
weeds, the program against A. filiculoides in southern Africa ranks among the most successful cases anywhere in the world.
Ó 2003 Elsevier Inc. All rights reserved.

Keywords: Stenopelmus rufinasus; Evaluation; Aquatic weeds; Azolla

1. Introduction field, Eastern Cape, South Africa). The combination of


a lack of natural enemies, dispersal between water bo-
Azolla filiculoides Lamarck (Azollaceae) (red water- dies by humans and possibly waterfowl, and phospho-
fern), a native of the American continent (Stergianou rus-enriched waters facilitated the dispersal and
and Fowler, 1990), is a small (1–2.5 cm), heterosporous, establishment of A. filiculoides (Hill, 1998a). In 1999,
floating, aquatic fern (Lumpkin and Plucknett, 1980). the weed was recorded at 152 sites in South Africa
It has spread to many countries where it is considered a (Henderson, 1999).
weed (Ashton, 1974; Diatloff and Lee, 1979; Hill, 1999). Azolla filiculoides forms dense mats (up to 20 cm
A. filiculoides was first recorded as a naturalized species thick) on slow-moving water bodies and on empound-
in South Africa in the Oorlogspoort River, near ments of up to 10 ha. The weed has had deleterious ef-
Colesberg (30°370 5700 S; 25°210 2100 E), Northern Cape fects on the biodiversity of aquatic ecosystems
Province in 1948 (Oosthuizen and Walters, 1961), after (Gratwicke and Marshall, 2001) and on water utilization
having been introduced as an ornamental fish-pond (Hill, 1997). The weed has increased siltation rates of
plant (R. Randall, Cape Nature Conservation, Sedge- dams and rivers, reduced the quality of water for agri-
cultural and domestic use, clogged irrigation canals and
*
Corresponding author. Fax: +27-11-403-1429.
pumps, and has led to the drowning of livestock that
E-mail addresses: ajmcconnachie@yahoo.com, rietamc@plant2. were unable to differentiate between pasture land and
agric.za (A.J. McConnachie). weed covered water bodies (Hill, 1997).

1049-9644/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved.
doi:10.1016/j.biocontrol.2003.08.010
A.J. McConnachie et al. / Biological Control 29 (2004) 326–331 327

Control options for red waterfern are limited. Me- 2. Materials and methods
chanical removal is impractical because of the rapid rate
of increase of the plant. The surface-area doubling time The weevils were mass-reared at the Plant Protection
of A. filiculoides is reported to be 7–10 days (Lumpkin Research Institute (PPRI), Rietondale, Pretoria, and at
and Plucknett, 1982). There are no registered herbicides the University of the Witwatersrand (Wits), Johannes-
for use against the plant in South Africa. Thus, the only burg, and then released at 112 sites between 1997 and
feasible, long-term solution is biological control (Hill, 2002. This total is about 40 sites less than the total
1997). After investigations of its biological control po- number of A. filiculoides sites listed by Henderson
tential in its native habitat (Center et al., 1992; Lumpkin (1999). Ongoing laboratory and field experiments,
and Plucknett, 1982; Richerson and Grigarick, 1967), however, indicated that S. rufinasus is an able disperser
the frond-feeding weevil Stenopelmus rufinasus was col- (McConnachie, 2003) and that these sites where weevils
lected on A. filiculoides in Florida (USA) and imported were not released, would soon be colonized.
into South Africa in 1995. Weevils were released either directly (during field
The biology of S. rufinasus was investigated by Hill trips by the authors), or mailed to the affected water-
(1998b), and is summarized below. The adult females users upon request. Initially, weevils were released in
deposit eggs singly in holes that they have chewed in the batches of 500. However, this number was found to be
frond tip. The hole is then covered with a cap of frass. excessive when we discovered that 100 weevils were
The females lay up to 325 eggs during their life-time. sufficient to establish a population. Weevils were most
Egg hatch is followed by three larval instars, all of which often collected as copulating pairs in the mass-rearing
feed voraciously on the fronds of A. filiculoides. The first facility, so an assumption was made that equal numbers
instars mine the upper frond lobes, while the second and of males and females were released (McConnachie,
third instars feed externally. Older larvae are each ca- 2003). Where possible, sites were visited twice annually
pable of consuming several plants per day. Pupation over a 4-year period. When site visits were not feasible,
commences with larvae chewing out a depression in an telephonic contact was maintained with the respective
A. filiculoides frond, above the water surface. Larvae landowners to ascertain the status of the weed. All sites
then enclose themselves within an ovoid, black chamber were visited at least once. A record was kept of weevil
made from anal secretions. The duration from egg hatch establishment and the impact of the weevils on the weed
to adult eclosion ranges from 16 to 23 days. (i.e., changes in area of the water body covered, time
Adult S. rufinasus are small weevils, about 2 mm long. taken for the weed to disappear, reappearance of the
They are a grey-black in colour and are covered with weed, and recolonization by the weevil). Details of
red, black, and white scales in a variable pattern. The tip weevil population dynamics and their effects on plant
of the rostrum and legs are reddish. The sexes are su- vigour were not collected at the field sites because these
perficially similar, but in the males the first abdominal data were recorded in field-cage studies (McConnachie,
sternite is flat or slightly concave at the midline, while it 2003). The effects of the weevils were recorded using
is strongly convex in females. Both sexes are relatively ÔbeforeÕ and ÔafterÕ fixed-point photographs at 20 sites.
long-lived (55–60 days). Forno and Julien (2000) proposed a scoring system to
Hill (1997) determined the host-specificity of S. ru- rate the success of phytophagous arthropods following
finasus on 26 species of plants in 15 families. The weevils their establishment as biological control agents against
did not feed or oviposit on the majority of plant species aquatic weeds. This system was adapted from Goeden
tested. S. rufinasus adults, however, were able to feed on (1983) and Harris (1991) and applied specifically to
all three species of Azolla tested (A. filiculoides, Azolla aquatic weeds. It was used in this study to compare the
pinnata R. Br., and Azolla nilotica Decne. Ex. Mett.), impact of S. rufinasus on A. filiculoides with other bio-
and oviposition and larval development occurred (Hill, logical control agents that have been used against other
1997). A. filiculoides was obviously the most suitable aquatic weeds elsewhere in the world.
host for the weevil, as significantly more larvae were
able to develop on it than on the other species. The
weevil was thus cleared for release in South Africa in 3. Results and discussion
December 1997 (Hill, 1998b).
The aim of this study was to assess the contribution of Stenopelmus rufinasus was released at 112 Azolla-in-
S. rufinasus to the control of A. filiculoides since its re- fested sites around South Africa (total surface area of
lease in South Africa. Post-release evaluation of biolog- 208.5 ha), and at one site (7 ha) in Zimbabwe (Table 1).
ical control agents is at best ad hoc, if it happens at all. Before the insects were fully established, the weed in-
The A. filiculoides program fortuitously brought together festations at 13 sites were washed away by floods, and a
money and manpower, with a rapidly establishing and dam at one site was prematurely drained. Eighty-one
effective agent which has allowed us to summarize the percent of all the field sites (91 sites), were completely
dramatic events of this very successful work. cleared of A. filiculoides by the weevils (i.e., 203.5 ha) in
328 A.J. McConnachie et al. / Biological Control 29 (2004) 326–331

Table 1
Records of Azolla-infested water bodies in South Africa and Zimbabwe where Stenopelmus rufinasus has been released, showing the success rate and
time to reach control
Province/country Area of Azolla No. of weevils No. sites Area of Azolla Mean time to control
infestation (ha) released controlled (%) cleared (ha) (months  SD)
Eastern Cape 77.3 4000 17 (89.5) 76.3 4.6  3.4
Free State 52.1 8500 33 (84.6) 49.1 7.4  3.8
Gauteng 20.5 4600 13 (92.90) 19.0 7.1  4.9
KwaZulu Natal 3.0 500 3 (60) 3.0 7.4  0.0
Limpopo 7.5 400 3 (75) 6.5 11.8  7.2
Mpumalanga 20.1 1600 5 (41.7) 16.6 5.5  4.2
Northern Cape 13.0 600 2 (50) 11.0 9.0  4.8
Western Cape 15.0 4200 12 (100) 15.0 6.4  4.8
Chiredzi 7.0 300 3 (100) 7.0 10.8  0.0
(Zimbabwe)
Totals/means 215.5 24,700 91 (81.3) 203.5 6.9  4.3

A B

C D

E F
Fig. 1. Before-and-after photographs of the impact of Stenopelmus rufinaus on Azolla filiculoides in the field in South Africa. Witmos, Eastern Cape
Province—312 days to clearance (A) and (B). Slykspruit River, Free State Province—271 days to clearance (C) and (D). Sasolburg Nature Reserve
Dam, Free State Province—270 days to clearance (E) and (F). Note secondary infestation of Wolffia sp., Spirodela sp., and Lemna sp. in foreground
of (F).
A.J. McConnachie et al. / Biological Control 29 (2004) 326–331 329

an average of 6.9 (4.3) months per site. The status of weevils disperse after causing local extinction of their
the remaining seven sites was not determined. Following host plant, but recolonize the original sites once the
destruction by the weevil, no A. filiculoides plants were plant populations recover (T. Center, United States
located at any of the sites that had been cleared by Department of Agriculture, Agricultural Research Ser-
S. rufinasus (Figs. 1A–F). At some sites, secondary in- vice, Fort Lauderdale, Florida, personal communica-
festations of Lemna sp. (Lemnaceae), Spirodela sp. tion). In addition, once the mat has collapsed, we have
(Lemnaceae), and Wolffia sp. (Lemnaceae) were apparent found quiescent adults on other aquatic vegetation and
(Fig. 1F), indicating that these sites were eutrophic, have been able to keep them alive for up to 2 months
probably as a result of human activities (Pieterse, 1993). without food (McConnachie, 2003). These individuals
After destruction by S. rufinasus, A. filiculoides re- are a potential source for weevil populations that re-
appeared at only 22 release sites, mostly in the Free colonize recovered mats of the host plant.
State Province (Table 2). The average time to reap- Two aspects of this biological control program seem
pearance of the weed was 12.2 (7.2) months. These to be unusual with respect to other weed control efforts.
reappearances could have been due to the germination First, S. rufinasus literally eradicated the weed at most of
of spores (Ashton, 1982; McConnachie, 2003) or due to the release sites that were not affected by flooding. No A.
the movement of whole plant material by waterfowl or filiculoides plants could be located at any of these sites
other agents. Each of the 22 sites was eventually recol- after control. Complete eradication of the target weed is
onized by S. rufinasus, unaided, and subsequently the very rare in biological control, and it is perhaps more
weed has been cleared again from 18 sites. This is similar accurate to refer to the observations in this study as
to the situation recorded in southern USA where the ‘‘local extinctions’’ of the weed. In the biological control

Table 2
Sites at which Azolla filiculoides reappeared subsequent to clearing by Stenopelmus rufinasusa
Locality Coordinates Time to reappearance (months) Damage to plant after relocationc
Eastern Cape Province
Graaf Reinet 32°030 4200 S 24°140 0200 E 6 Damaged
Witmos (Cradock) 32°310 1200 S 25°360 4800 E 18 Controlled
Molteno 31°120 3400 S 26°350 1700 E 13 Controlled

Free State Province


Bethulie (Zoetvlei) 30°300 2400 S 25°530 3300 E 18 Damaged
Bethulie (Iona) 30°290 5100 S 25°470 1200 E 15 Controlled
Harrismith GC 28°150 4700 S 29°070 4400 E 12 Controlled
Harrismith Dam 28°160 5200 S 29°060 4300 E 13 Controlled
Slykspruit 30°130 5500 S 26°050 4900 E 12 Controlled
Smithfield 3026 BA 14 Controlled
Viljoenskroon 27°100 2100 S 26°550 3000 E 20 Controlled
Westminster 29°120 5600 S 27°120 5800 E 17 Controlled

Gauteng Province
Marievale 26°210 2700 S 28°300 5500 E 2 Controlled
Midrand 25°570 3600 S 28°090 5100 E 7 Controlled
Limpopo Province
Rust de Winter 25°130 4200 S 28°290 4800 E 3 Controlled
Mpumalanga Province
Bethal 26°270 0500 S 29°270 4100 E 6 Controlled
Messina 2230 AC 5 Controlled
Potchestroom 26°430 7500 S 27°040 0200 E 3 Controlled
Northern Cape Province
Colesburg 30°370 5700 S 25°210 2100 E 7 Damaged
Western Cape Province
George East 33°590 4700 S 2°310 1800 E 9 Damaged
Steenberg 34°040 3500 S 18°250 3800 E 19 Controlled
Noordhoek 34°070 1400 S 18°220 5400 E 31 Controlled
Wynberg 34°010 2400 S 18°290 2300 E 19 Controlled
Summary Reoccurrence at 22 sites 12.2(7.2)b months 18 sites controlled
a
All 22 of these sites were relocated by the weevils and the extent of the damage they inflicted on the host plant is also recorded.
b
Mean (SD).
c
‘‘Damaged’’—weed turns purple; visible larval feeding damage. ‘‘Controlled’’—weed completely cleared by the weevil.
330 A.J. McConnachie et al. / Biological Control 29 (2004) 326–331

of insect pests, local extinctions are considered to deliver Agricultural Research Council. John Hoffmann, Sue
satisfactory control in model systems, as opposed to the McConnachie, and Cliff Moran are thanked for com-
classical stable-target-equilibrium model in biological ments on the manuscript. Farmers from all over South
control theory (Murdoch et al., 1985). Second, biological Africa are thanked for their hospitality and participa-
control usually requires a number of years before its ef- tion. Dr. G. Buckingham (USDA-ARS, Florida, USA)
fects are fully realized (McFadyen, 1998). In this pro- is thanked for collecting and sending starter colonies of
gram, water bodies were cleared of A. filiculoides in 7 S. rufinasus.
months on average. Cilliers (1991a) reported similar
clearance times (ranging from 9 to 10 months) in South
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