Biological Invasions

, Volume 11, Issue 3, pp 619–624

Comparing the effects of the exotic cactus-feeding moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) and the native cactus-feeding moth, Melitara prodenialis (Walker) (Lepidoptera: Pyralidae) on two species of Florida Opuntia

Authors

  • Amanda J. Baker
    • Department of BiologyUniversity of South Florida
    • Department of BiologyUniversity of South Florida
Original Paper

DOI: 10.1007/s10530-008-9276-4

Cite this article as:
Baker, A.J. & Stiling, P. Biol Invasions (2009) 11: 619. doi:10.1007/s10530-008-9276-4

Abstract

This study examined the effects of the native cactus moth borer, Melitara prodenialis, and the invasive cactus moth borer, Cactoblastis cactorum, on two common cactus species, Opuntia stricta and O. humifusa at coastal and inland locations in central Florida. Opuntia stricta were present only at coastal sites and O. humifusa were present at coastal and inland sites. Throughout the duration of the study, coastal plants were subject to damage solely by C. cactorum and inland plants solely by M. prodenialis. Results showed marginally significantly higher numbers of eggsticks on O. stricta than O. humifusa and significantly higher numbers at coastal sites than at inland sites. There was also significantly higher moth damage on O. stricta than O. humifusa and at coastal sites than inland sites, but not significantly so. However, there was a higher level of plant mortality for O. humifusa than for O. stricta and a significantly higher level of cactus mortality at inland sites when compared to coastal sites. This increased mortality may be due to increased attack by true bugs, Chelinidea vittiger, and by Dactylopius sp., combined with attack by M. prodenialis. Inland plants also tended to be smaller than coastal plants and could be more susceptible to the combined effects of all insects. Further long-term research on coastal cactus survival when attacked and unattacked by Cactoblastis is necessary to fully determine the effects of this moth on Opuntia survival.

Keywords

Cactoblastis cactorumMelitara prodenialisOpuntia humifusaO. strictaMortality of native cacti

Introduction

The arrival of Cactoblastis cactorum into North America has caught the attention of many individuals. The moth was first documented in Florida in 1989 and has spread to coastal Georgia, South Carolina, Alabama and Mississippi. In 2006 it was found on two barrier islands off the Yucatan coast of Mexico. There is concern how the moth will affect the ornamental cactus industry if it spreads to the US desert southwest (Irish 2001), what levels of damage the moth will inflict upon commercial agriculture crops throughout Mexico (Soberon et al.2001), and what impact it will have on the natural Opuntia communities in the US southwest and Mexico (Stiling 2002). The response of cactus to infestation by C. cactorum is key to answering such questions.

To date, there has been little attempt to quantify the damage to and the mortality of common southeastern US cacti, such as O. stricta and O. humifusa, when exposed to attack by C. cactorum. Johnson and Stiling (1998) demonstrated an increase in the number of C. cactorum damaged O. stricta in central Florida and an increase in death rates over a 2-year period, 1991 through 1993, but their sample sizes were very small. The Florida populations of O. stricta and O. humifusa have now been exposed to C. cactorum for more than 15 years, and it is appropriate to re-examine the effect of C. cactorum on Florida cacti to better quantify its effects.

A complicating factor is that there exists a common native cactus moth borer, Melitara prodenialis, whose larvae also feed on the internal tissues of prickly pear cladodes. The damage appears similar to that caused by C. cactorum. Melitara prodenialis larvae are easily distinguished from C. cactorum larvae by opening infested pads. Cactoblastis cactorum larvae are bright orange with black spots and a black head capsule. Melitara prodenialis larvae are a dark indigo blue and have a brown head capsule. The early instars of both species can be pale in color with small black spots, but the color of the head capsules allows for accurate identification at these stages. The eggsticks of M. prodenialis are also easily distinguished from those of C. cactorum in the field, for they are usually found in shorter chains and the eggs are more squat or flattened than those of C. cactorum (Johnson and Stiling 1996 and pers. obs.). Furthermore, at the time of this study, C. cactorum was found primarily at coastal sites, not at our inland sites used here, and M. prodenialis was found mainly at inland sites, and not at our coastal sites used here. This study reports on a 2-year monitoring program comparing the effects of cactus moths on cacti at coastal and inland locations, which in essence was a comparison of the effects of invasive C. cactorum and native M. prodenialis on native cacti.

Methods

Study plants

The two most common cacti in Florida are O. stricta Haworth and Opuntia humifusa Rafinesque. Opuntia stricta is a large plant species that grows erect and is found only in coastal areas, often among sea oats and other dune vegetation and along shell mounds. The cladodes can be quite large, up to 25 cm in length (Wunderlin and Hansen 2003) and are often slightly ovate with rounded edges. The spines are short, yellow, often clustered and can be up to 4 cm long. An older plant can grow up to one and a half meters tall and can have a mostly woody “trunk”. The formation of lignified woody tissue in cacti naturally occurs with age, but can also be induced by injury to the tissue, including that caused by insects (Gibson and Nobel 1986).

Opuntia humifusa are much shorter than O. stricta and can be found along coastal dunes and shell mounds as well as on inland sandhill and scrub areas. The cladodes of O. humifusa are more round when compared with O. stricta cladodes and measure between 4 and 16 cm in length (Wunderlin and Hansen 2003). The spines are longer, usually singular and can be gray, white or darkly colored. Spines may occasionally be absent. Opuntia humifusa tends to be more recumbent than O. stricta, but seems to have a slightly more erect presentation in inland areas than along the coast, growing up to 30 cm in height (pers. obs.). This species can also have woody pads when older. Both cactus species may have plants ranging in size from only a few pads up to 200.

Cactus moth life histories

Cactoblastis cactorum (Berg) is a pyralid moth, native to South American countries such as Uruguay, Paraguay, Argentina and parts of Brazil (Mann 1969). The moth specializes on the platyopuntia subfamily of cacti (Dodd 1940; Mann 1969), which are known as the prickly pears. The eggs of the adult moth are laid in a stick, one on top of the other, often at the tip of a cactus spine (Hoffmann and Zimmermann 1989) but they may also be adhered directly to a cladode or a fruit (pers. obs.). The female will lay more than one eggstick before her death in approximately 10 days. The number of eggs found in an eggstick can range from 5 to 100 with an average of about 50 eggs (Hoffmann and Zimmermann 1989). Once hatched, the tiny, gray larvae cooperatively chew through the tough outer cuticle of the cladode and enter the pad. The larvae are gregarious and feed inside the cladodes, consuming all but the vascular tissue (pers. obs.). As they feed, the larvae push frass out of holes in the cladode. This dripping or weeping may be used as a good indicator of active plant infestation in the field. During the day, it is common to see C. cactorum larvae congregated on the outside of the cactus plant (Dodd 1940), presumably to escape the hot internal temperatures that can be greater than 55°C when exposed to sunlight (Gibson and Nobel 1986). When larval development is complete, larvae usually drop into the soil or litter at the base of the plant to pupate, although they may also use an empty cladode “shell” (Habeck and Bennett 1990). Once the adult moths emerge, they begin to mate. In subtropical Florida, C. cactorum peak larval activity occurs between March and October, but larvae are visible at other times throughout the year at lower densities (pers. obs.). The generation time in Florida has not been determined, but Florida moths probably have at least three generations per year (Habeck and Bennett 1990, pers. obs.). In central Florida, at our study areas, only C. cactorum occurred at coastal locations, it was present at some inland sites, but never attacked our study plants.

Melitara prodenialis (Walker) is a pyralid moth native to Florida and the eastern United States. This is another cactus borer specializing on the playopuntia family of cacti. In Florida, the moth has three generations per year. The adults first emerge in March or April, generation two occurs in June, and the last generation appears between August and October (Mann 1969). Melitara prodenialis adult females also lay their eggs in a “stick” similar to C. cactorum. The eggsticks of M. prodenialis are shorter than the eggsticks of C. cactorum. They contain between 30 and 50 eggs, with an average of 30 (Mann 1969). Melitara prodenialis eggsticks are oviposited to most parts of the plant; directly on a cladode, at the end of a spine, on a fruit and even at a segment joint (pers. obs.). The larvae of M. prodenialis range from a light gray to a bright blue color when mature. Melitara prodenialis larvae also collectively feed on the internal tissues of the prickly pear, but they are rarely seen on the outside of the plants (pers. obs.). The larvae will pupate in the same manner as C. cactorum, in an empty cladode or at the base of the plant in the litter (Mann 1969). In central Florida, at the time of our study, M. prodenialis occurred only at inland locations.

Plant damage and mortality levels

In July 2003, 200 O. humifusa plants were marked at each of three island sites along the Lake Wales Ridge; Lake Wales Ridge State Forest, Crooked Lake Prairie and Archbold Biological Research Station. Two hundred plants were also marked at two coastal locations; Honeymoon Island State Park and Lido Beach, and 100 plants were marked at a third coastal location; Fort de Soto Park. Coastal sites contained a mix of O. stricta and Opuntia humifusa. All plants were monitored for 2 years. Site visits occurred monthly from July 2003 through July 2005.

On all plants, the presence of stem-boring cactus-moth larvae and eggsticks of both native and exotic species was noted and species identified. When eggsticks were present, the number of eggs was counted using a hand lens and notation was made if the eggstick was hatched or unhatched. When larvae were present, the number of pads that showed active damage was counted. Plant size, as determined by pad number, was measured monthly and a yearly average pad number was obtained for each cactus. Plant mortality over the 2-year census period was determined. The presence of other insect herbivores such as true bugs, Chelinidea vittiger, and cochineal insects, Dactylopius spp., was also recorded.

Differences in plant quality between locations were determined by analyzing nitrogen content. Plant pads were collected from 30 randomly selected plants at each site in July 2004, except Fort de Soto, where only 15 plants were sampled. The samples were brought back into the lab and were dried and ground with a Wiley mill. The nitrogen content was determined using a CE Instruments NC 2100 CN Analyzer (CE Elantech, Lakewood, NJ, USA). In addition, soil cores were collected approximately 10 cm deep within 6 inches from the base of 30 randomly selected plants at each of the six sites, in June 2004, except Fort de Soto, where only 15 soil samples were collected. Opuntia roots are oriented horizontally, between 5 and 15 cm below the soil surface; therefore our soil samples were collected from appropriate depths (Gibson and Nobel 1986). The samples were brought back into the lab and the nitrogen content was analyzed using a CE Instruments NC 2100 CN Analyzer (CE Elantech, Lakewood, NJ, USA).

All data were tested for normality with a Kolmogorov–Smirnov test, and variables that met the assumptions of normality were compared between cactus species and between inland and coastal sites using Student’s t-tests. All statistical analysis was performed using Systat 11.0 (Systat Software, Inc. 2004). Plant mortality was made normal via a square root transformation. Non-normal data sets were compared with Mann–Whitney tests.

Results

Coastal versus inland locations

There was a significant difference among the number of eggsticks over the 2-year period between coastal and inland locations, with a higher average at coastal sites than at inland sites (Table 1). This suggests that C. cactorum either lays a greater number of eggs, or simply has a much larger population than does Melitara prodenialis. The percentage of damaged plants was over twice as large at coastal sites than inland sites but the difference was not significant.
Table 1

Differences in cactus moth egg stick density, damage to Opuntia plants, plant mortality and plant and soil nitrogen between coastal and inland locations. Means and standard errors given

Attribute

Location

P-value

Coastal

Inland

Eggstick density/500 plants

0.23 ± 0.05

0.03 ± 0.03

0.005

% Plants damaged

43.70 ± 0.16

15.00 ± 0.19

0.119

% Pads damaged

6.10 ± 0.04

1.80 ± 0.02

0.148

Average number of pads per plant

34.19 ± 12.9

17.89 ± 11.2

0.172

% Plant mortality—all plants

3.80 ± 0.03

12.70 ± 0.02

0.017

% Plant nitrogen

0.551 ± 0.09

0.811 ± 0.17

0.080

% Soil nitrogen

0.171 ± 0.07

0.091 ± 0.03

0.162

% Plants damaged by true bugs

51.70 ± 0.09

63.50 ± 0.47

0.688

% Plants damaged by Dactylopius spp.

30.30 ± 0.27

58.00 ± 0.37

0.349

% Damaged plant survival

96.50 ± 0.05

92.80 ± 0.07

0.476

The percentage of damaged pads was also much greater at the coast than inland although this difference was not statistically significant. This result is likely an accurate representation of moth activity since the sample sizes were 7,852 pads on the coast and 8,857 pads inland. Coastal plants were larger than inland plants, having over 50% more pads. Surprisingly, inland sites showed a significantly higher level of mortality than did coastal sites. There was no significant difference in plant nitrogen and soil nitrogen between the two locations with coastal sites having lower plant nitrogen but higher soil nitrogen values. True bug and Dactylopius damage were higher at inland locations than coastal locations, but not significantly so. Even after cacti had been damaged by Cactoblastis or Melitara, plant survival was high, over 90%, and did not differ between locations.

Opuntia humifusa at coastal versus inland sites

We also compared attack rates and mortality levels of O. humifusa only between coastal (N = 331) and inland sites (N = 600) (Table 2). Once again there was a greater number of eggsticks deposited on O. humifusa plants at the coast than those inland (Table 2), again indicating C. cactorum may lay more eggs than does Melitara prodenialis. Both the percentage of damaged O. humifusa plants and the percentage of damaged pads were higher at the coast, but not significantly different between the two locations. Once again, coastal plants tended to be larger and plant mortality was greater inland than along the coast. Plant and soil nitrogen were significantly or marginally significantly higher at the coast than inland. There were no differences in attack rates by other insects. Damaged plant survival was not affected by location.
Table 2

Differences in cactus moth eggstick density, damage to O. humifusa plants, plant mortality and plant and soil nitrogen between coastal and inland locations

Attribute

Location

P-value

Coastal

Inland

Eggstick density/500 plants

0.12 ± 0.02

0.03 ± 0.03

0.005

% Plants damaged

27.50 ± 0.18

15.00 ± 0.19

0.456

% Pads damaged

2.70 ± 0.02

1.80 ± 0.02

0.672

Average number of pads per plant

31.20 ± 11.8

17.89 ± 11.2

0.229

% Plant mortality–all plants

3.50 ± 0.04

12.70 ± 0.02

0.022

% Plant nitrogen

0.531 ± 0.07

0.811 ± 0.17

0.057

% Soil nitrogen

0.177 ± 0.03

0.091 ± 0.03

0.033

% Plants damaged by true bugs

73.10 ± 0.24

63.50 ± 0.47

0.768

% Plants damaged by Dactylopius spp.

48.90 ± 0.42

58.00 ± 0.37

0.793

% Damaged plant survival

78.00 ± 0.36

92.80 ± 0.07

1.000

Means and standard errors given

Opuntia stricta versus O. humifusa at coastal sites

Finally, we also compared moth activity and plant mortality at coastal sites between O. stricta (N = 169) and O. humifusa (N = 331). The average number of eggsticks that were counted on plants was marginally significantly different between the two species (Table 3), with higher numbers of eggs laid on O. stricta. The percentage of pads damaged by moth larvae was significantly different between the two species; with significantly greater damage to O. stricta. Over three-quarters of the 169 O. stricta plants at the coast were damaged by C. cactorum at some point during the 2-year duration of the study and this was significantly higher than the damage levels on O. humifusa. Opuntia stricta plants were generally much bigger than O. humifusa. Plant mortality was minimal at the coast and did not differ between species. There was no significant difference in plant or soil nitrogen between the plant species. The abundances of true bugs and Dactylopius were both much higher on O. humifusa than O. stricta. Plant survival following Cactoblastis damage was high.
Table 3

Differences in cactus moth eggstick density, damage to plants, plant mortality and plant and soil nitrogen between O. stricta and O. humifusa at coastal locations

Attribute

Species

P-value

O. stricta

O. humifusa

Eggstick density/500 plants

0.474 ± 0.23

0.12 ± 0.02

0.060

% Plants damaged

75.40 ± 0.21

27.50 ± 0.18

0.039

% Pads damaged

6.90 ± 0.02

2.70 ± 0.02

0.055

Average number of pads per plant

57.37 ± 25.14

31.20 ± 11.83

0.178

% Plant mortality-all plants

2.90 ± 0.05

3.50 ± 0.04

0.872

% Plant nitrogen

0.306 ± 0.30

0.531 ± 0.07

0.275

% Soil nitrogen

0.199 ± 0.10

0.177 ± 0.03

0.748

% True bug damage

7.10 ± 0.08

73.10 ± 0.24

0.011

% Plants damaged by Dactylopius spp.

0.6 ± 0.01

48.90 ± 0.42

0.246

% Damaged plant survival

88.90 ± 0.19

78.00 ± 0.36

0.487

Means and standard errors given

Discussion

Attack rates of coastal cacti by C. cactorum were greater than those of inland cacti by Melitara prodenialis. Cactoblastis cactorum did not attack any plants marked at our inland study locations throughout the duration of the study. In the course of the study C. cactorum was noted at three inland study locations: Archbold Biological Research Station, Crooked Lake Prairie and Hickory Lake Scrub. Similarly, at the coastal sites, C. cactorum was the only cactus feeding moth identified; M. prodenialis was not encountered. It is not clear entirely whether these preferences are for habitat or plant species. Cactoblastis cactorum attacks both O. stricta and O. humifusa at the coast but prefers O. stricta. O. stricta are not present inland. Attack rates of O. humifusa are higher at the coast than inland.

When all marked plants from both O. stricta and O. humifusa were considered together, the number of eggsticks laid and the percentage of moth-damaged plants was much higher at the coast, than inland. Thus, we predicted plant mortality would be higher at the coastal sites than inland sites. To our surprise, inland sites showed a higher proportion of plant mortality. Similar results were observed when we compared O. humifusa at coastal and inland locations and we must ask why. First, coastal cacti were somewhat larger, in terms of numbers of pads, and may be more resistant to the ravages of cactus moths. Some of this size difference is driven by the fact that O. stricta are larger cacti than O. humifusa, and O. stricta are found only at the coast. However, coastal O. humifusa are also larger than their inland counterparts. Both C. cactorum and M. prodenialis require only about four pads for the development of an entire eggstick (Johnson and Stiling 1996). However, there were often multiple eggsticks on plants. Larvae from several eggsticks could kill smaller cacti, such as inland O. humifusa, but would be much less likely to kill larger coastal O. stricta. In support of this idea, coastal O. humifusa showed higher mortality rates than O. stricta. Second, there was a higher level of mealybug (Dactylopius spp.) infestation and true bug infestation at inland sites over coastal sites and this could have increased cacti mortality rates inland. Much of this difference was driven by a preference of these insects for O. humifusa. Third, lower plant nitrogen levels in coastal plants could have resulted in higher per capita feeding by caterpillars, increasing damage levels. Fourth, the 2004 hurricane season was very active. The inland sites were more heavily affected by storms. The storms brought high levels of rainfall. In particular, a category four hurricane passed through the inland area in August of 2004. This resulted in standing water present at some sites although our analyses showed only 1% of all inland cacti died after sustaining some form of hurricane damage. Coastal sites never had standing water. All these factors could have increased inland plant mortality though we could not definitively score mortality from these different factors.

On the coast, the primary stress to Opuntia cacti came from C. cactorum. It is still possible that in the absence of Dactylopius spp., true bug infestation, and hurricane-related mortality, Cactoblastis could cause higher cactus mortality at coastal sites than Melitara at inland sites, though separate experiments would be needed to determine this. At present, Cactoblastis is not causing high mortality of cacti, though it is causing high levels of damage and is probably reducing cactus size. Further long-term observations on cacti attacked and unattacked by C. cactorum and M. prodenialis in similar locations will be necessary to compare their effects on Opuntia size, survival and reproduction.

Acknowledgements

Financial support was provided by NSF grant DEB 03-15190. We are grateful to the staff at Lake Wales Ridge State Forest, Crooked Lake Prairie, Archbold Biological Research Station, Honeymoon Island State Park, Lido Beach Park and Fort de Soto Park for allowing us to work at these sites.

Copyright information

© Springer Science+Business Media B.V. 2008