Demise and Recolonization by the Tropical Fire Ant and Other Ants (Hymenoptera: Formicidae) in a Melon Field in Mexico¹

The tropical fire ant, Solenopsis geminata F. (Hymenoptera: Formicidae), is an important invasive species worldwide (CABI Compendium 2022, doi.org/10.1079/cabicompendium.50568; Sanchez-Peña et al. 2005, Entomol. News 116: 363–366). It is also a key predator of pests in agroecosystems such as maize (Zea mays L.) (Risch and Carroll 1986, J. Ecol. 67: 1319–1327), tropical orchards (Eskafi and Kolbe 1990, Environ. Entomol. 19: 148–153), and rice (Oryza sativa L.) (Way and Heong 2009, Bull. Entomol. Res. 99: 503–512) and can provide substantial reductions in populations of specific pests. Herein, we report on the population changes, as indicated by foraging activity, of S. geminata in a conventionally managed commercial muskmelon (Cucumis melo L. var. reticulatus) field with intensive pesticide and agrichemical use. Our objective was to obtain baseline data on changes in fire ant populations in response to crop phenology and agricultural practices from transplanting until harvest.

The study was conducted at Santa Isabel, municipality of Cadereyta, Nuevo León state, Mexico (25°28′33′′N, 100°00′31′′W). The climate is subtropical dry, with a total precipitation of 600–800 mm/yr (National Institute of Statistics and Geography 1983, Secretaria de Programacin y Presupuesto, Mexico), and a mean temperature of 26°C (range, 25–42°C). The 1.5-ha muskmelon field was bordered on the eastern and western sides by weedy hedgerows (Fig. 1) occupied by pigweed, Amaranthus sp.; bitter weed, Parthenium hysterophorus L.; sunflower, Helianthus annuus L.; and bermudagrass, Cynodon dactylon (L.) Persoon. Senescent unplowed fields were <30 m to the north (1.5-ha tomato [Solanum lycopersicum L.] field) and <30 m to the east (3.0-ha cabbage [Brassica oleracea L.] field; Fig. 1). Concurrent sampling of the two senescent fields during our study showed that S. geminata was a widespread, extremely abundant, and highly dominant aggressive predator of insects there during the test. This fire ant is native in the area (Sanchez-Peña et al., 2009, Fla. Entomol. 92: 107–115).

Muskmelon was established (transplanted) on the first week of April 2023 on black plastic mulch. Conventional intensive horticultural agriculture and frequent applications of pesticides occurred throughout the study until harvest. Although we were not able to obtain detailed records of pesticides applied to the crop, we determined that chlorpyrifos and neonicotinoids were applied at least several times during crop development.

We used 0.4-cm sections of pork hot dogs (FUD®, Sigma Alimentos, Monterrey, Mexico) as baits for estimating field ant foraging activity. Hot dog baits are highly effective for sampling Solenopsis invicta Buren foragers (Bao et al. 2011, Appl. Entomol. Zool. 46: 165–169). On each sampling date, we placed baits at 5 p.m.–6 p.m. because ant activity was very low earlier in the day due to high temperature and intense sunshine. This time of day also allowed us to measure diurnal activity of thermophilic ants (i.e., Forelius spp.) as well as that of less thermophilic diurnal and nocturnal ants (i.e., S. geminata). Stringer et al. (2011, Environ. Entomol. 40: 1276–1284) exposed hot dog baits for 60 min for fire ant sampling; however, we chose a 30-min period because exposure for >30 min resulted in some scavenging by birds, crickets (Gryllidae), and earwigs (Dermaptera). This time period was sufficient for complete colonization of baits by ants, whereas longer periods sometimes led to partial or complete bait retrieval, interspecific competition, and displacement of one ant species by another at the baits.

Sampling dates were 30 April, 24 May, and 16 August 2023. The gap of time between the second and third sampling was due to “row closure” (canopy closure) in June and July making walking and sampling in the field impossible without significant damage to plants. At this point, agrichemical application had shifted from foliar sprays to irrigation under the plastic mulch. Harvest was complete, and there were no further pesticide applications were suspended at least 2 wks before 16 August.

On each sampling date, three linear transects were placed in the field: west, central, and east (Fig. 1). Ten baits were placed 3.5 m apart in each transect (30 per transect). Also, 15 baits were placed 3.5 m apart in linear transects in each weedy hedgerow on the eastern and western sides of the field.

Ant counts from the first sampling were used to develop visual estimates of the numbers of ants on baits. Therefore, in the first sampling only, baits with ants were quickly picked up and preserved in 70% ethanol. The ants were subsequently counted. From these counts, numbers of ants on baits were estimated in the field, expressed as 5, 20, 50, 100, 150, or 200 ants/bait; that is, a bait fully covered with ants was given an estimate of 200 ants/bait.

Data were examined via the Shapiro–Wilk test for assumptions of parametric analysis (McDonald 2014, Handbook of Biological Statistics, 3rd ed., Sparky House Publishing, Baltimore, MD). If assumptions were not met, nonparametric tests were used: initially Kruskal–Wallis (KW) one-way analysis of variance for comparison among transects inside the field followed by post hoc multiple comparison Dunn’s test (Statistics Kingdom 2022, https://statskingdom.com/kruskal-wallis-calculator.html). Differences in tendency and distribution in total numbers of ants in the field and the surrounding hedgerows combined were compared using the permutation algorithm EDISON-WMW for calculation of a P value via the exact Wilcoxon–Mann–Whitney (WMW) test (Marx et al. 2016, Genom. Proteom. Bioinform. 14: 55–61). When <50% baits were occupied by ants, leading to an abundance of zero counts (McElduff et al. 2010, Adv. Physiol. Edu. 34: 128–133), the Fisher–Freeman–Halton (FEP) exact probability test (http://vassarstats.net/textbook/index.html) was used to determine whether nonrandom associations existed between transects and baits. Similarities in ant numbers between hedgerows and their respective adjacent transect in the field (east or west) were tested for all ants (WMW test) and for each species (FEP test).

Ant numbers in Fig. 2A–E are estimated values derived from visual observations on baits as described. Ants of any species were absent from the baits within the melon field on the first two sampling dates (Fig. 2A, 30 April and 24 May). On the same dates, there was an abundance of ants in the adjacent senescent tomato and cabbage fields, where >80% of the baits were often colonized by S. geminata after 30 min.

We postulate that the absence of foraging ants (all species) in the melon field on the first two sample dates was due to application of insecticides or cultivation and preparation of the field for planting or other agricultural practices. Stringer et al. (1980, J. Ga. Entomol. Soc.15: 413–417) documented significant reductions in S. invicta populations after single soil applications of acephate and chlorpyrifos (both organophosphate insecticides). Helms et al. (2021, Environ. Entomol. 50: 1276–1285) observed increased ant activity after crop harvest in the midwestern United States. They indicated that the impact of planting insecticide-coated seed and applications of other insecticides and agrichemicals likely suppressed ant populations during the growing season. Melon production in Mexico often involves repeated applications of potent neurotoxic insecticides (Mendoza-Bonfilio 2023, Med. Int. Mex. 39: 692–695) in greater amounts than in maize and wheat production in the midwestern United States. Ant populations in agricultural production fields may be impacted by topical toxicity of pesticides as well as bottom-up ecological effects such as shortage of prey (Helms et al. 2021) or lack of seeds resulting from weed control that are important food items for S. geminata (Risch and Carroll 1986, J. Ecol. 67: 1319–1327). In addition, the negative effect of plowing and crop soil physical preparation on ant populations cannot be ignored; however, our personal observations indicate that these local practices do not result in long-lasting ant annihilation as observed.

We observed a recolonization of the melon field by ant species in the 16 August sample (Fig. 2A, B). Helms et al. (2021) also reported recolonization, with increased ant activity at the end of the crop growing season (i.e., 75% of all ant foraging activity observed throughout the growing season occurred after harvest).

In our samples from the melon field on 16 August, 955 S. geminata were found on 40% of the baits (n = 0–200 [estimated ant number range in parentheses]) and 160 Forelius cf. pruinosus (Roger) foragers were on 10% of the baits (n = 0–100). In the west and east hedgerows, there were 905 S. geminata on 60% of the baits (n = 0–200), 100 F. cf. pruinosus on 13.3% of the baits (n = 0–50), and 300 Pheidole tetra Creighton on 26% of the baits (n = 0–100). The total ants (all species) foraging activity differed significantly when comparing within-field activity to that in the hedgerows combined (WMW test: P = 0.00237; Fig. 2B). However, no significant differences were detected in comparing activity of each species within the field with activity in the hedgerows combined (FEP test: P = 0.4238 for S. geminata and P = 1.0 for F. cf. pruinosus). Significant differences in activity occurred among the east, central, and west transects within the field (KW test: H = 8.81, df = 2, P = 0.01). (Please note that the KW test does not compare means, but rather the distributions of data ranks in treatments.) The Dunn’s post hoc statistic indicates that there were no significant differences in total ants between the east and west transects (Z = 0.3459, P = 0.7294). By contrast, there were significant differences in total ants between the west transect and the central transect (Z = 2.679, P = 0.0025) and between the east transect and the central transect (Z = 3.016, P = 0.0073). Therefore, the analysis confirms that the differences between the inside and outside the field are due to the lack of ants in the center of the field and their presence toward the margins.

When comparing S. geminata activity among the three in-field transects, we found overall significant differences in numbers of baits occupied by S. geminata (FEP test: P_A = 0.0290, P_B = 0.0145). There were no significant differences in numbers of occupied baits by S. geminata between the east and the west transects (P = 0.3698) and between the west and the central transects (P = 0.1679). There were significant differences between the east and the central transects (FEP test: P = 0.0197). In comparing the foraging activity in each hedgerow with that in adjacent in-field transects, we found no significant differences in the total numbers of ants in the west hedgerow and in the adjacent west in-field transect (P = 0.0708; Fig. 2C) and between the east hedgerow and the adjacent east in-field transect (P = 0.6011; Fig. 2D; both WMW test). Likewise, there were no significant differences in activity of each species between the west hedgerow and the adjacent west in-field transect (FEP test: P = 0.2406 for S. geminata, P = 1 for F. cf. pruinosus) and between the east hedgerow and the adjacent east in-field transect (FEP test: P = 0.1789 S. geminata, P = 1 for F. cf. pruinosus). When comparing the west and the east hedgerows, there were no significant differences in total worker numbers for all species combined (WMW test: P = 0.06047; Fig. 2E) or for individual species (S. geminata and F. cf. pruinosus; FEP test: P = 1 and P = 0.11, respectively). Therefore, for the last sampling date, the lack of statistical significance in ant presence (total number of ants and that of S. geminata and F. pruinosus individually) between the two hedgerows, between the east hedgerow and east in-field transect, and between the west hedgerow and the west in-field transect (Fig. 2C–E) indicates gradual distribution of ants from the margins to the center of the field.

In summary, a clear and rather uniform recolonization of ants of the melon field was observed following melon harvest and cessation of pesticide applications and other agricultural activities. Furthermore, the recolonization appeared to originate from the weedy hedgerows on the eastern and the western sides of the field. At this time, ant foraging activity and species presence in the eastern and the western sides of the field closely resembled those in the adjacent hedgerows, whereas the central area of the field remained relatively devoid of ant foraging activity. In addition, the numbers of foraging ants (total and by species) were not significantly different between the two hedgerows, which were separated by 120 m.

Santos et al. (2018, Basic Appl. Ecol. 33: 58–65) reported that ant community diversity in sugarcane was reduced within fields and was inversely related to distance from undisturbed wild vegetation (forest) fragments. Ant communities of the sugarcane fields and forest fragments were more similar later in the season than directly after sugarcane harvest, suggesting gradual recolonization of the fields from the fragments. Likewise, our data indicate recolonization of the melon field from weedy, small, natural vegetation islands (hedgerows). Morandin et al. (2014, Agric. Ecosyst. Environ. 189: 164–170) also detected that 3- and 7-m-wide hedgerows were an important source of beneficial predatory insects, including Hymenoptera and ground-dwelling Staphylinidae, and positively impacted pest management in adjacent tomato fields.

In conclusion, our observations indicate that there might be a significant depletion of the ant fauna, including cornerstone predators such as S. geminata, in some horticultural fields in Mexico. The factor(s) driving this depletion are not known with certainty, but are possibly insecticides applied to the crop. Adjacent weedy hedgerows appear to be a significant source of predatory ant populations that recolonized the field in this study. These observations indicate that ecosystem services might be severely impacted under some horticultural production regimes in Mexico and that local discussion toward the implementation of integrated pest management strategies be in place.