Temperature-dependent development and life tables of Palpita unionalis (Lepidoptera: Pyralidae)

1 Introduction

Olive (Olea europaea L.; Oleaceae) farming has expanded and intensified from its traditional distribution area in Mediterranean countries. Furthermore, olives are being planted in areas where climatic conditions differ markedly from that ideal for its growth and production to face the progressive global demand for both olive oil and olives. Over the last fifty years, the acreage dedicated to olive orchards has tripled, with cultivation practices adopted in 56 countries, some of which have climates quite different from the traditional olive-producing regions. Despite these challenges, olive farming has been making inroads in the southeastern United States. Particularly in Florida, a state better known for its citrus groves, the olive industry is emerging as a viable agricultural endeavor. This expansion into Florida, along with areas of South Carolina, Georgia, Alabama, and Mississippi, signifies a notable shift in olive cultivation, embracing regions that mirror the latitudes of successful groves in Texas (Sánchez-Martínez and Garrido-Almonacid 2019). Insect pests are one of the limiting factors for olive expansion and production, affecting both established and emerging growth areas.

The olive leaf moth, Palpita unionalis Hubner (Lepidoptera: Pyralidae), is one of the main pests of olive groves. There are reports of 156 Palpita species worldwide, but only a few are of economic importance and P. unionalis is the most prominent (Scheunemann et al. 2021). This pest used to be one of the secondary pests of olives; nevertheless, it is now considered a main pest, especially in nurseries and young plantations. Additionally, it has become more significant in mature olive trees. Synonyms of P. unionalis are Margaronia unionalis (Hubner) or Palpita vitrealis (Rossi) (Yilmaz and Genc 2012). P. unionalis also attacks other genera of the family Oleaceae including Jasminum, Ligustrum, Phillyrea, and Fraxinus (Athanassiou et al. 2004; Tzanakakis 2003), hence the pest has an alternative common name “Jasmine moth”. Larvae also attack leaves and flower buds of ornamentals (Hegazi et al. 2007). The pest usually has a moderate population density in olive orchards; however, sporadic outbreaks happen, inflicting severe damage in olive orchards and nurseries (Hegazi et al. 2012; Kovanci and Kumral 2004; Kovanci et al. 2006). Larvae attack tender leaves and buds, where neonate larvae feed upon the lower surface parenchyma, turning the leaves dry and brown. When P. unionalis feeds on apical buds in nurseries, stunted growth of seedlings occurs. Usually, infested flower buds abscise before fruit set. In the case of heavy infestations, the larvae attack olive fruits, particularly the table varieties, eating the fruit sometimes right down to the stone, which makes them unacceptable for the market (Athanassiou et al. 2004; Badawi et al. 1976; Kumral et al. 2007). The most significant damage takes place in nurseries, young olive trees, and shoots of old trees (Khaghaninia and Pourabad 2009). Feeding damage may reach 90 % of the leaf area in nurseries and young orchards, and in older fruiting orchards, the reduction of olive production may reach up to 30 %, especially in the fruit ripening time of late summer and early fall (Arambourg 1986; López-Villalta 1999).

Several research studies have focused on the biological aspects of P. unionalis with respect to general biology (Badawi et al. 1976; Khaghaninia and Pourabad 2009; Shehata et al. 2003; Yilmaz and Genc 2012), population fluctuations (Hegazi et al. 2011, 2012; Kovanci et al. 2006), and life tables on various hosts (Kumral et al. 2007). However, the effect of temperature on these biological aspects is not yet well known. Temperature plays a significant role in insect development, survival, reproduction, behavior, fitness, abundance, and distribution (Barbosa et al. 2019). Accordingly, the study of temperature effects on insect life-history variables is crucial to predict pest occurrence and to develop effective management strategies (Kang et al. 2009; Nava et al. 2007). Consequently, the objective of the present study was to gain a better understanding of P. unionalis thermal demands and to elucidate the effect of temperature on its growth, survival, and reproductive success for better prediction and management of this pest.

2 Materials and methods

This study was done at the Laboratory of Entomology of the Desert Research Center (Cairo, Egypt), under controlled conditions of temperature, relative humidity (RH, 70–80 %) and photoperiod 16:8 h (L:D).

3 Results

3.1 Biology of P. unionalis at different temperatures

The duration of all P. unionalis developmental stages, and the survival of larval stages were found to be temperature dependent (Table 1). Out of all the evaluated temperatures, 17 °C significantly prolonged the developmental periods for eggs (from when the egg is laid until the larvae hatches; 7.8 days) (F = 42.37; df = 5; P < 0.01), larvae (from when the larvae hatches until it pupates; 43.0 days) (F = 53.96; df = 5; P < 0.01) and pupae (from when the pupae is formed until the adult emerges; 27.0 days) (F = 37; df = 5; P < 0.01). In contrast, at 30 °C the shortest developmental periods were recorded for egg (3.0 days) and pupal (6.0 days) stages. The shortest developmental period for the larval stages was at 27 °C (15.4 days), which did not significantly differ from the developmental period at 30 °C (18.9 days). Furthermore, larval survival (17.1 %) was negatively affected at 30 °C when compared to the other considered temperatures (F = 53.96; df = 5; P < 0.01). Nevertheless, no statistical differences related to temperature were detected regarding egg (F = 0.69; df = 5; P < 0.63) and pupal (F = 2.02; df = 5; P < 0.09) survival.

Table 1:

Biological parameters of Palpita unionalis at different temperatures (mean value ± SE).

Biological parameters		Temperature (°C)
		17	20	22	25	27	30
Duration (days)	Egg stage	7.82 ± 0.13a	5.28 ± 0.08b	3.88 ± 0.13c	3.67 ± 0.10c	3.42 ± 0.21cd	3.01 ± 0.01d
	Larval stage	43.00 ± 3.33a	22.44 ± 0.55b	22.08 ± 0.83b	17.20 ± 0.35bc	15.35 ± 0.69bc	18.93 ± 0.65bc
	Pupal stage	27.03 ± 0.34a	11.85 ± 0.17b	9.51 ± 0.09c	7.75 ± 0.12d	8.06 ± 0.09d	6.02 ± 0.33e
Survival (%)	Egg stage	82.72 ± 5.50	86.79 ± 3.63	93.19 ± 4.13	85.51 ± 4.23	79.22 ± 7.86	83.20 ± 2.38
	Larval stage	89.11 ± 6.58a	63.64 ± 7.43ab	40.22 ± 10.15b	58.46 ± 5.01b	47.14 ± 7.10b	17.14 ± 2.53c
	Pupal stage	68.00 ± 8.00	69.58 ± 8.87	81.86 ± 4.69	90.00 ± 3.27	78.33 ± 8.33	60.71 ± 9.67
Fecundity		229.00 ± 9.87ab	586.25 ± 148.25a	144.29 ± 69.00b	260.77 ± 58.37ab	434.50 ± 69.55ab	81.00 ± 62.28b
Pre-oviposition period		3.00 ± 0.58	2.00 ± 0.00	2.71 ± 0.57	2.15 ± 0.41	3.13 ± 0.35	3.29 ± 0.47
Oviposition period		17.00 ± 1.73a	14.75 ± 2.06a	4.57 ± 0.81b	6.85 ± 1.03b	6.75 ± 0.65b	2.14 ± 0.83b
Post-oviposition period		2.33 ± 0.67	2.50 ± 0.65	4.57 ± 1.90	2.00 ± 0.44	1.88 ± 0.23	2.43 ± 0.90
Sex ratio		0.516 ± 0.09	0.528 ± 0.06	0.430 ± 0.05	0.500 ± 0.06	0.462 ± 0.05	0.537 ± 0.07

1. Rows without letters had no significant differences by the F-test (P ≤ 0.05). Means (±SE) followed by the same letters in the row did not differ by Tukey’s test (P ≤ 0.05). The sex ratio values did not differ by temperature regime according to pairwise comparison test of proportions (P ≤ 0.05). Fecundity is number of eggs. Oviposition periods in days. Sex ratio was determined by calculating number of female/(female + male) of the emerged adults.

For adult moths, females kept at 20 °C had the highest fecundity, 586.3 eggs which significantly reduced to 81.0 eggs at 30 °C (F = 4.95; df = 5; P < 0.01). Females presented the longest oviposition period at 17 °C (17.0 days), which did not significantly differ from the oviposition period recorded at 20 °C (14.8 days). All other temperatures significantly reduced the oviposition period (F = 17.09; df = 5; P < 0.09). Meanwhile, the durations of both pre-oviposition (F = 1.24; df = 5; P < 0.31) and post-oviposition (F = 1.161; df = 5; P < 0.35) periods were not significantly affected by temperature. The sex ratio at all temperatures was close to 0.5 and with no significant differences (Z = 0.20; P < 0.01).

Regarding female longevity (χ ²  = 46; df = 5; P < 0.01; Figure 1A) and male longevity (χ ²  = 20.7; df = 5; P < 0.01; Figure 1B), survival was inversely proportional to temperature. Females lived longer than males at all the tested temperatures. Females survived until 27 days (mean survival time “MST” = 17 days) and males survived until 21 days (MST = 14 days) at the lowest temperature 17 °C. Longevity of both females and males was significantly shortened to 11 days (MST = 7 days) and 10 days (MST = 5 days) at the highest temperature 30 °C, respectively, compared to the other tested temperatures.

Figure 1:

Survival curves for females (A) and males (B) of Palpita unionalis reared at different temperatures. Vertical dotted lines represent the mean survival time (MST) for each temperature. Curves followed by the same letters for each sex (see figure key) did not differ from one another by the log-rank test.

All the life table parameters (Table 2) significantly differed at the evaluated temperatures. For net reproductive rate (R ₀; F = 13.63, df = 5; P < 0.01), intrinsic rate of increase (r _m; F = 6.72, df = 5; P < 0.01), finite rate of increase (λ; F = 6.77, df = 5; P < 0.01), generation time (T; F = 25.51, df = 5; P < 0.01) and doubling time (DT; F = 5.73, df = 5; P < 0.01). It was possible to observe the variation of the R ₀ from 105.7 to 35.5 and T from 37.0 days to 31.6 days at 20 and 30 °C, respectively. Despite the values of r _m and λ (0.136; 1.145) being the highest at 25 °C, these values did not significantly differ from those calculated for the lower temperatures. Meanwhile, the highest DT value (6.2) was recorded for the P. unionalis kept at 30 °C.

Table 2:

Influence of six different temperatures on the life table parameters of Palpita unionalis.

Parameter	Temperature (°C)
	17	20	22	25	27	30
Net reproductive rate (R 0)	77.83 ± 12.37ab	105.72 ± 3.69a	92.30 ± 4.74a	75.79 ± 6.40ab	59.29 ± 5.32bc	35.53 ± 3.19c
Intrinsic rate of increase (r m) (day−1)	0.120 ± 0.006ab	0.126 ± 0.003ab	0.135 ± 0.002a	0.136 ± 0.002a	0.122 ± 0.003ab	0.113 ± 0.003b
Finite rate of increase (λ) (day−1)	1.127 ± 0.007ab	1.134 ± 0.004ab	1.145 ± 0.002a	1.145 ± 0.002a	1.130 ± 0.003ab	1.119 ± 0.003b
Generation time (T) (day)	36.21 ± 0.42a	36.98 ± 0.78a	33.40 ± 0.15b	31.84 ± 0.61b	33.33 ± 0.01b	31.56 ± 0.05b
Doubling time (DT) (day)	5.83 ± 0.32ab	5.50 ± 0.14ab	5.12 ± 0.08b	5.11 ± 0.08b	5.67 ± 0.12ab	6.15 ± 0.16a

1. Means (±SE) followed by the same letters in the row do not differ by Tukey’s test (P ≤ 0.05).

4 Discussion

Studying the thermal requirements of pests can help to improve their monitoring, define their initial existence, and predict their population outbreaks (Scheunemann et al. 2021). These data can also help in the development of model-based risk assessment tools, such as distribution maps (Azrag and Babin 2023). This knowledge could be helpful for the development of suitable management strategies that support the effectiveness of biocontrol programs and that rationalize the use of potentially harmful synthetic pesticides. In the present study, overall, the parameters measured for the biology of P. unionalis concur with the findings of many authors who studied the same pest with variations that may be attributed to factors like diet and environmental conditions. In laboratory studies, Fouda (1973) and Badawi et al. (1976) found that the incubation period lasted between 3 days at 30 °C to 12 days at 15 °C, and all larvae failed to hatch at 35 °C. Moreover, the duration of the last (6th) larval instar (5–7 days at 25 °C) was nearly twice that of the first instar (3 days at 25 °C). The intermediate larval instars were the lowest in duration and all larvae died at 35 °C after the first molt. The pupal stage lasted for 23.4, 15.7, 7.5, and 7.0 days for females and 31.2, 17.1, 8.5, and 8.0 days for males at 15, 20, 25 and 30 °C, respectively. Vassilaina-Alexopoulou and Santorini (1973) recorded 21–26 days of larval development at 26 °C. El Khawas (2000) observed that the larvae hatch within 1–3 days after deposition at 25 °C. The mean duration of larval development was 15.8 days, and the total developmental period (from egg to adult) was 23.4 days. The developmental time of immature stages was 30 days at 25 °C (Kumral et al. 2007). Khaghaninia and Pourabad (2009) recorded 34.9 days for the mean total developmental time at 27 °C. Yilmaz and Genc (2012) reported 4.16 days incubation period and 23.3 days for larval development at 24 °C.

The current results showed that the lower temperatures favored the survival of adults and larval stages of P. unionalis, yet eggs and pupal stages were not significantly affected. This was in support of Yilmaz and Genc (2012), who recorded 60 % larval survival at 24 °C compared to 59 % larval survival at 25 °C during the present study. There were also similarities in adult female survival as Yilmaz and Genc (2012) recorded 16 d of survival and females survived for 15 d in our study. Kumral et al. (2007) found the immature survival at 25 °C to be 73 % and the mean number of deposited eggs was 390 eggs. This was similar to the fecundity recorded by Yilmaz and Genc (2012), 352 eggs at 24 °C, but higher than the number of eggs that we recorded, 260 eggs at 25 °C. However, the fecundity (586 eggs) as well as the net reproductive rate, R ₀ (105), were the highest at 20 °C during our study. This was similar to the results obtained by Scheunemann et al. (2021) for Palpita forficifera Munroe as its highest net reproductive rate, 121, was recorded at 25 °C as compared to its values, 21, 81, and 99 at 15, 20, and 30 °C, respectively. The net reproductive rate expresses the ability of the population to grow with each succeeding generation, and it is a crucial marker of population dynamics that sums up the insect physiological potential for reproduction (Kumral et al. 2007; Richards 1961). The comparison between these net reproductive rates along different temperatures allows evaluation of the potential for population increase under climate stress. The present results reveal the high biotic potential of the olive leaf moth at 22 °C, where this rate was significantly reduced at high temperatures. It is worth to note that adverse unstable climate and the presence of natural enemies out in the field are important limiting factors of this biotic potential (Scheunemann et al. 2019). All the other demographic parameters obtained from the current study indicate a negative impact of high temperature on P. unionalis.

In conclusion, higher temperature negatively affected the growth, survival, and reproduction of the olive leaf moth. This was observed from the evaluated biological parameters and the calculated life table parameters. However, despite developing at a slower rate, P. unionalis subjected to the lowest temperature, 17 °C did not differ significantly from those kept at slightly higher temperatures for other biological and life table parameters. Nevertheless, the biological parameters recorded for P. forficifera revealed that the ideal temperatures for development were 25 and 30 °C (Scheunemann et al. 2021). This variation in heat preferences between the two species may be due to the difference in their range of distribution. P. unionalis was reported to spread in the Mediterranean region, and P. forficifera presents in South America (Ricalde et al. 2015; Scheunemann et al. 2019). This was confirmed as the lower thermal threshold of P. unionalis in the present experiments for the egg to adult period was 7.10 °C, but it was 10.7 °C for P. forficifera (Scheunemann et al. 2021). According to the reported thermal requirements of P. unionalis, the number of annual generations should be calculated for each region separately. A lower number of generations are expected to be found in regions where the temperature is lower. In general, P. unionalis seems to be a multivoltine species that has many overlapping generations throughout the year (Hegazi et al. 2007). López-Villalta (1999) reported asynchronous development of larvae due to temperature, which resulted in concurrent presence of all stages throughout the season. Future studies are needed to conduct field observations of pest activity as temperature variations in the field differ from the constant temperatures used in the laboratory. The ecological relationship between the pest and its host plant (olive) also should be considered. The web formed by larvae, for example, during the feeding process may provide a suitable microclimate, allowing the larvae to survive critical periods, especially extreme cold and hot weather conditions (Scheunemann et al. 2021). Still, considering the expected scenario of global climate change that proposes temperature rising, the biology, thermal regime and number of generations are expected to change. This requires continuous monitoring of the bioecological behavior of the pest and the change of its thermal requirements for the future safety of global olive production.