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Impact of dietary restriction on development, mating, and reproduction in the natural predator Pardosa pseudoannulata

Published online by Cambridge University Press:  07 October 2024

Xiaoming Wang
Affiliation:
Hubei Key Laboratory of Regional Development and Environmental Response, Faculty of Resources and Environmental Science, Hubei University, Wuhan, China State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan, China
Wei Li
Affiliation:
Hubei Key Laboratory of Regional Development and Environmental Response, Faculty of Resources and Environmental Science, Hubei University, Wuhan, China
Li Song
Affiliation:
State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan, China
Zuojun Xie
Affiliation:
State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan, China
Jie Liu
Affiliation:
Hubei Key Laboratory of Regional Development and Environmental Response, Faculty of Resources and Environmental Science, Hubei University, Wuhan, China
Yao Zhao*
Affiliation:
State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan, China
Yu Peng*
Affiliation:
Hubei Key Laboratory of Regional Development and Environmental Response, Faculty of Resources and Environmental Science, Hubei University, Wuhan, China
*
Corresponding authors: Yao Zhao; Email: [email protected]; Yu Peng; Email: [email protected]
Corresponding authors: Yao Zhao; Email: [email protected]; Yu Peng; Email: [email protected]
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Abstract

Dietary restriction-influenced biological performance is found in many animal species. Pardosa pseudoannulata is a dominant spider species in agricultural fields and is important for controlling pests. In this study, three groups – a control group (CK group), a re-feeding group (RF group), and a dietary restriction group (RT group) – were used to explore development, mating, reproduction, and the expression levels of Vg (vitellogenin) and VgR (vitellogenin receptor) genes in the spider. The findings indicated that when subjected to dietary restriction, the carapace size, weight of the spiderlings, and weight of the adults exhibited a decrease. Furthermore, the preoviposition period and egg stage were observed to be prolonged, while the number of spiderlings decreased. It was also observed that re-feeding reduced cannibalism rates and extended the preoviposition period. Dietary restriction also affected the expression of the Vg-3 gene in the spider. These results will contribute to the understanding of the impact of dietary restriction in predators of pest control, as well as provide a theoretical foundation for the artificial rearing and utilisation of the dominant spider in the field.

Type
Research Paper
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

Introduction

Food shortage is common in the lives of many animal species, owing to the spatial and temporal variability of food supplies in nature (Mehner and Wieser, Reference Mehner and Wieser1994; Zhu et al., Reference Zhu, Song, Chen, Yun, Zhang, Zhao and Peng2023). Starvation is essentially a physiological reaction to a change in food obtained, such as a shift from an abundant to a scarce food supply (McCue, Reference McCue2010). The effect of dietary restriction on animals was first discovered in rodents and has already been proven in yeast, nematodes, flies, mice, and other animals (Jiang et al., Reference Jiang, Jaruga, Repnevskaya and Jazwinski2000; Carey et al., Reference Carey, Liedo, Harshman, Zhang, Müller, Partridge and Wang2002; Pletcher et al., Reference Pletcher, Macdonald, Marguerie, Certa, Stearns, Goldstein and Partridge2002; Mair et al., Reference Mair, Goymer, Pletcher and Partridge2003; Cooper et al., Reference Cooper, Mockett, Sohal, Sohal and Orr2004). Juvenile starvation has been shown to impact the developmental period, with consequences on adult size, reproductive success, and adult functional response (Boggs and Niitepõld, Reference Boggs and Niitepõld2016; Wang et al., Reference Wang, Kaftanoglu, Brent, Page and Amdam2016). For example, the effects of different hunger levels on the lacewing Chrysoperla carnea were varying; a higher hunger level led to a longer time to process food (Hassanpour et al., Reference Hassanpour, Maghami, Rafiee-Dastjerdi, Golizadeh, Yazdanian and Enkegaard2015) and some spiders were also able to prolong longevity under dietary restrictions (Austad, Reference Austad1989; Kasumovic et al., Reference Kasumovic, Brooks and Andrade2009). In contrast, individuals may react to starvation by increasing their food intake to alleviate the negative impact (Hector and Nakagawa, Reference Hector and Nakagawa2012; Regalado et al., Reference Regalado, Cortez, Grubbs, Link, van der Linden and Zhang2017; Paul et al., Reference Paul, Singh, Dennis and Müller2022), and growth recovery based on starvation and re-feeding is a growth strategy in specific species (Xavier et al., Reference Xavier, Megarajan, Balla, Sadu, Ranjan, Babu, Ghosh and Gopalakrishnan2023). Previous studies have showed growth recovery with different food restriction-influenced growth performance in some insects, such as silkworms, Bombyx mori, and the moths, Orgyia antiqua (Esperk and Tammaru, Reference Esperk and Tammaru2010; Dai et al., Reference Dai, Feng, Mao, Gu, Bian, Sun, Li, Wei and Li2022). As an important predatory natural enemy of farmland, spiders play a key role in field to control pest (Zhu et al., Reference Zhu, Song, Chen, Yun, Zhang, Zhao and Peng2023). Although some studies have showed that starvation or food restriction may cause substantial changes in spiders (Segoli et al., Reference Segoli, Lubin and Harari2007; Lichtenstein et al., Reference Lichtenstein, DiRienzo, Knutson, Kuo, Zhao, Brittingham, Geary, Ministero, Rice, David, Scharf and Pruitt2016), whether the spiders recovery growth when they resume feeding after restricted food needs further investigation.

The response of animal growth to limited supplies of food differs by species. Depending on the degree of recovery, growth recovery may be classified into three types: (1) over-recovery, in which multiple cycles of deprivation and re-feeding result in a weight gain that surpasses that of what the species is fed normally (Hayward et al., Reference Hayward, Noltie and Wang1997), (2) complete recovery, in which previously restricted species acquire the same body mass as normally fed species (Kim and Lovell, Reference Kim and Lovell1995; Jobling and Johansen, Reference Jobling and Johansen1999), and (3) partial recovery, in which food-restricted species grow faster after resuming regular feeding, but do not acquire the same body mass as normally fed species (Weatherley et al., Reference Weatherley, Gill and Casselman1987; Paul et al., Reference Paul, Paul and Smith1995). For instance, recovery growth studies showed that starvation in golden pompano, Trachinotus ovatus, juveniles resulted in complete and partial growth recovery (Liu et al., Reference Liu, Luo, Chen, Tan, Zhang and Li2015), and in Indian pompano, Trachinotus mookalee, juveniles displayed complete growth recovery (Xavier et al., Reference Xavier, Megarajan, Balla, Sadu, Ranjan, Babu, Ghosh and Gopalakrishnan2023). Yip and Lubin (Reference Yip and Lubin2016) examined the potential for dietary compensation through alterations in foraging behaviour in the orb-weaving spider Cyrtophora citricola. The researchers discovered that the spiders were incapable of compensating for diet restriction by modifying their foraging behaviour. To date, few studies have explored the effects of dietary restriction on the mating, reproduction, and gene expressions of spiders (Yip and Lubin, Reference Yip and Lubin2016).

In addition to growth performance and reproduction, gene expression can also be affected by growth recovery in the animal (Chatzifotis et al., Reference Chatzifotis, Papadaki, Despoti, Roufidou and Antonopoulou2011; Qi et al., Reference Qi, Yang, Li, Xia, Wang, Huang and Chen2016). For sea bass, Dicentrarchus labrax, gonad size was reduced and vitellogenesis was hindered (Chatzifotis et al., Reference Chatzifotis, Papadaki, Despoti, Roufidou and Antonopoulou2011). A previous study has reported that the expression level of insulin-like growth factor-1 in Mongolian sheep, Ovis arie, was increased in a re-feeding condition, and that there was no significant difference from the control group (Yang et al., Reference Yang, Wu, Qi, Hou and Yang2007). Vitellogenin (Vg) is endocytosed into oocytes via the vitellogenin receptor (VgR), which is critical for Vg accumulation and oocyte maturation (Tufail and Takeda, Reference Tufail and Takeda2009; Mitchell et al., Reference Mitchell, Sonenshine and Pérez de León2019). VgR is essential for ovarian development and egg-laying in oviparous species (Schneider, Reference Schneider1996).

The wolf spider, Pardosa pseudoannulata (Araneae: Lycosidae), primarily feeds on a variety of agricultural pests such as planthoppers, leafhoppers, and other Lepidoptera pests (Preap et al., Reference Preap, Zalucki, Jahn and Nesbitt2001; Wang et al., Reference Wang, Song and Zhu2006; Huang et al., Reference Huang, Quan, Wang, Yun and Peng2018). It is wide-spread, has a high adaptability to its environment, and is commonly found in moist habitats at the edges of bodies of water (Yang et al., Reference Yang, Peng, Tian, Wang, Wei, Xie and Wang2018, Reference Yang, Lu, Wu, Yu, Xu, Han and Liu2022; Wang et al., Reference Wang, He, Peng, Wang and Song2021; Lv et al., Reference Lv, Yang, Wang, Zeng, Li, Tang, Wang and Song2021b). Spiders are an important biological factor in the natural control of pests, playing a strategic role (Yang et al., Reference Yang, Song, Xu, Zhou and Shi2021; Fu et al., Reference Fu, Jing, Pan, Zhu, Feng, Liu and Xiao2022; Zhang et al., Reference Zhang, Wen, Li and Li2023); however, insecticides have been used to control arthropod pests all over the world (Oerke, Reference Oerke2006; Guedes et al., Reference Guedes, Smagghe, Stark and Desneux2016), which could lead to a reduced food supply for spiders. One previous study has shown that growth recovery exists in the spiders, Pardosa prativaga, and can lead to changes in growth (size and weight) and reproduction (Jespersen and Toft, Reference Jespersen and Toft2003), therefore, the impact of dietary restriction on development, mating, reproduction, and gene expression of P. pseudoannulata needs to be explored.

In this study, we used dietary restriction to imitate a possible starvation condition. We set up three groups: a control group (CK group), a restriction group (RT group), and a recovery feeding group (RF group) to explore whether growth recovery would occur when P. pseudoannulata returned to normal feeding. The spiders were assessed for growth and development, reproduction, and the expression levels of Vg and VgR genes under these three treatments. Our findings may contribute to the understanding of dietary restriction in predators of pest control.

Materials and methods

Spider collection and rearing

P. pseudoannulata carrying egg sacs were collected in July 2021 in rice fields from Hanchuan County in the Xiaogan District in Wuhan, Hubei Province, China. The spiders were reared to the third generation in a climate-controlled room in Hubei University. The hatched spiderlings were reared individually in glass tubes (20 mm diameter, 90 mm high) with a moistened sponge at the bottom, and were fed fruit flies (Drosophila melanogaster) and midges (Chironomidae) every 3 days. The fruit flies were bred and reared in the laboratory, and midges were collected from the shores of Shahu Lake. The rearing conditions were maintained at 25 ± 1°C and 65 ± 5% relative humidity under a 14:10 h light:dark (L:D) photoperiod.

Experimental design

Newly hatched spiderlings were divided into three different feeding protocols: a CK group (n = 60), a RT group (n = 60), and a RF group (n = 60), and each spiderling was kept separately in a glass tube without competition or cannibalism. The spiderlings in the three treatment groups were fed a combination of midges and fruit flies every 3 days, with the RF and RT groups obtaining half the amount of food as the CK group. The adult spiders in the three treatment groups were only fed fruit flies twice a week, and the amount of feeding in the RT group was half of that in the CK and RF groups. The feeding amounts of spiders at different instars are shown in table S1.

Impact of dietary restriction on development, mating, and reproduction

After the spiderlings hatched from the egg sacs, the development of the spiderlings was observed daily. The carapace length (distance from the foremost end to the end of the head carapace) and carapace width (distance of the widest part of the head carapace) of spiderlings were measured under a stereo microscope (SZX7, Olympus, Tokyo, Japan) after moulting in different instars in each group. Meanwhile, the weight of the spiderlings in different instars after moulting and the adult spiders after maturation on days 0, 7, 14, 21, and 28 were measured using an electronic balance (BT1251, Sartorius Scientific Instruments, Beijing, China) in each group. The spiders were returned to its original specific glass tube after finishing all measures to avoid impacting their behaviour or feeding habits.

Female and male spiders in each treatment group were randomly selected for mating after 4 weeks of spider maturity. The female spider was placed in the mating box (100 mm diameter, 18 mm high), habituated to the surface of the filter paper for 30 min, then the male was gently put into the mating box and timing began. The male and female spiders were permitted to remain in the mating box for 20 min post-mating to observe sexual cannibalism. All the spiders are in a state of satiety for the mating experiment. The mating success rates, cannibalism rates, mating latency period (the time when males are introduced to the mating box to the time when males and females begin mating), and the mating duration (the time from when the male begins to mate until it dismounts the female) were recorded for each group of spiders. Mating failure occurs when the spiders do not begin mating within 30 min. Afterwards, the female spiders of successful mating were kept to rear, and the preoviposition period (the time from the end of mating to when the female lays eggs), the egg stage (the time from the beginning of the egg laying until the egg sac hatches), and the number of spiderlings in the first egg sacs of each female were recorded in the three different groups. The replicates in each treatment were: the CK group (n = 33), the RT group (n = 32), and the RF group (n = 33).

Sample preparation, RNA extraction, and cDNA synthesis

The adult spiders were carefully collected after maturation on days 0, 7, 14, 21, and 28 to determine Vg and VgR gene expression levels on different days. Samples were immediately frozen using liquid nitrogen and stored at −80°C prior to subsequent experiments. Each experimental treatment consisted of four biological replicates, with two spiders in each replicate.

Total RNA was extracted from the samples mentioned above using the RNAiso Reagent (TaKaRa, Maebashi, Japan), according to the manufacturer's instructions. RNA integrity was further evaluated using electrophoresis on a 1% agarose gel and quantified on a Nano-Drop 2000 (Thermo Scientific, Waltham, MA, USA). cDNA was synthesised from 1 μg total RNA using the Hifair®II 1st Strand cDNA Synthesis SuperMix for RT-qPCR (Yeasen, Wuhan, China) and kept at −20°C until further use.

Real-time quantitative polymerase chain reaction

Real-time quantitative polymerase chain reaction (RT-qPCR) was performed in 20 μl reaction mixtures containing MonAmp™ RT-qPCR Mix (Mona Biology Co., Ltd), 0.8 μl each of gene-specific primers, and a cDNA template. As shown in table S2, primers were designed as described in a study by Yang et al. (Reference Yang, Lu, Wu, Yu, Xu, Han and Liu2022). The reference gene used was the 18S ribosomal RNA of P. pseudoannulata (Lv et al., Reference Lv, Wang, He, Zeng, Tang, Li, Chen, Wang and Song2021a; Li et al., Reference Li, Li, Zhang, Sang, Peng and Zhao2024). The reaction conditions for RT-qPCR were as follows: an initial denaturation at 95°C for 30 s, followed by 40 cycles of 95°C for 5 s, 60°C for 30 s, and 7°C for 30 s. For the melting curve analysis and to guarantee the consistency and specificity of the amplified products, a temperature of 95°C for 30 s was utilised. Normalisation of cDNA levels was performed using 18S ribosomal RNA and the 2−ΔΔCt method for analysis.

Statistical analysis

The data were analysed after ensuring that they satisfied the assumptions for parametric analyses by the Kolmogorov–Smirnov test and the Levene's test (normal distribution of residuals and homogeneity of error variances). A two-factor repeated measures analysis of variance (ANOVA) was also used to analyse the carapace length and width, and weight. A one-way ANOVA with the least significant difference test was also used to analyse the number of spiderlings, and relative gene expression levels in the spiders. The chi-squared (χ2) test was used to analyse the mating and cannibalism rates of the spiders. The Kruskal–Wallis test was used to analyse the mating latency period, mating duration, preoviposition period, and incubation period of the spiders. SPSS v.26.0 software (IBM Corp., Armonk, NY, USA) was used for all data analyses.

Results

Development

As shown in fig. 1, with the increase of instar, different treatments had significant effects on the size and weight of juvenile spiders. As shown in fig. 2, dietary restriction significantly affected the body weight of adult spiders, and re-feeding restored the weight of adult females, indicating that dietary restriction significantly inhibited the growth and development of juvenile spiders.

Figure 1. Biological characteristic parameters of spiderling P. pseudoannulata: (a) carapace length, (b) carapace width, and (c) weight. The data are shown as mean ± standard error and are used to analyse by two-factor repeated measures analysis of variance (ANOVA).

Figure 2. Weight of adult P. pseudoannulata. (a) weight of female, (b) weight of male. The data are shown as mean ± standard error and are used to analyse by two-factor repeated measures analysis of variance (ANOVA).

According to the results of repeated measurement ANOVA, the interaction effect between instar and group is significant. With the increase of instar, the carapace length of the three treatment groups significantly changed (F 8, 262 = 7.231, P < 0.01). The carapace length in the CK group was significantly higher than that in the RF (P < 0.01) and RT groups (P < 0.01), but there was no significant change in the RF and RT groups (P = 0.641). The carapace width in the three treatment groups had significant changes (F 8, 262 = 8.676, P < 0.01), and the carapace width in the CK group was larger than that in the RF (P < 0.01) and RT (P < 0.01) groups, but there was no significant change in the RF and RT groups (P = 0.764). The weight of juvenile spiders in the three treatment groups had significant changes (F 8, 262 = 8.499, P < 0.01), and the weight of juvenile spiders in the CK group was higher than that in the RF (P < 0.01) and RT groups (P < 0.01), but there was no significant change in the RF and RT groups (P = 0.839).

With the increase of day, the weight of female adult spiders in the three treatment groups had a significant change (F 8, 80 = 1.364, P < 0.01). The weight of female adult spiders in the CK group was not altered compared to that in the RF group (P = 0.190), and the weight of female adult spiders in the RT group was significantly lower than that in the CK group (P < 0.01), but there was no significant difference between the RF and RT groups (P = 0.183). The weight of male adult spiders in the three treatment groups also had significant changes (F 8, 80 = 0.286, P = 0.047). The weight of male adult spiders in the CK group was significantly different from that in the RF (P = 0.012) and RT groups (P = 0.014), but there was no significant difference in the RF and RT groups (P = 0.966).

Mating and reproduction

Dietary restriction did not affect the mating success rate, mating latency, and mating duration of adult spiders, but increased the preoviposition period and the egg stage of spiders. Re-feeding significantly reduced the cannibalism rate, increased the preoviposition period and the number of spiderlings. As shown in fig. 3, the mating rates of P. pseudoannulata in each group had no significant differences (χ2 = 0.163, P = 0.922); however, the cannibalism rates of spiders in the RF group were significantly decreased, compared with the CK and RT groups (χ2 = 8.422, P = 0.015). For mating latency period (H 2, 84 = 0.210, P = 0.900) and mating duration (H 2, 84 = 2.072, P = 0.355), there were no significant differences in spiders between the three treatment groups (fig. 4A, B). Compared with the CK group, both the preoviposition period (H 2, 84 = 23.745, P < 0.001) and the egg stage (H 2, 84 = 22.789, P < 0.001) of spiders were significantly increased in the RF and RT groups (fig. 4C, D). In contrast, the number of spiderlings (F 2, 84 = 62.402, P < 0.001) of P. pseudoannulata in the RF and RT groups were significantly lower than that in the CK group (fig. 4E).

Figure 3. Mating success rates and cannibalism rates of adult P. pseudoannulata. The data are shown as mean ± standard error. The different lowercase letters indicate significant differences among each group.

Figure 4. Reproduction parameters of P. pseudoannulata: (a) mating latency period, (b) mating duration, (c) preoviposition period, (d) egg stage, and (e) number of spiderlings. The data are shown as mean ± standard error. The different lowercase letters indicate significant differences among each group.

Gene expression analysis

The expression levels of the Vg and VgR genes were investigated, and the results showed that dietary restriction affected Vg-3 gene expression. Upon maturation, the relative expression levels of the Vg-3 gene (F 2, 8 = 6.749, P = 0.020) were significantly increased in the RT group compared to the CK and RF groups on day 7; however, there were no significant differences in the relative expression levels of the Vg-1, Vg-2, Vg-3, and VgR-1 genes of spiders on the other days in the three treatment groups (all Ps > 0.05) (fig. 5).

Figure 5. Relative expression levels of the VgR-1 and Vg genes of P. pseudoannulata in each group after maturation. The data are shown as mean ± standard error. The different lowercase letters indicate significant differences among each group.

Discussion

According to previous studies, dietary restriction can lead to low energy levels obtained from food, which can lead to malnutrition and growth retardation, and may even negatively affect animal reproduction. The deficiency of food directly affects the normal physiology of animals, the reproductive performance of animals, and eventually leads to the negative impact of low offspring quality (Liu et al., Reference Liu, Luo, Chen, Tan, Zhang and Li2015), but there are few studies on the impact of dietary restrictions on animal mating and reproduction. This study used different dietary restriction treatments to investigate the effects on the development, mating, reproduction, and Vg and VgR gene expression of spiders. The findings indicated that when subjected to dietary restriction, the carapace size, weight of the spiderlings, and weight of the adults exhibited a decrease. Furthermore, the preoviposition period and egg stage were observed to be prolonged, while the number of spiderlings decreased.

In the present study, the carapace length, carapace width, and weight of the spiderlings in the RF and RT groups were significantly lower than those in the CK group from the 5th to 7th instars, indicating that food supply is one of the important factors that influence the growth and development of P. pseudoannulata. A previous study showed that the size of the orb-weaving spider, C. citricola, was smaller under food restriction than under control conditions (Yip et al., Reference Yip, Levy and Lubin2017), consistent with our results. However, after returning these food-limited spiders to a food-unrestricted condition, our results showed that there was no significant difference in weight between the female spiders under this condition and the female spiders without food restriction. This indicates that there is a phenomenon of growth recovery in females of P. pseudoannulata. For the wolf spider, Lycosa tarantula, individuals that were food-limited as spiderlings developed at a slower rate than food-unrestricted females, but acquired weight faster as adults, such that the weight of both treatments was comparable 2 weeks after maturity (Moya-Laraño et al., Reference Moya-Laraño, Orta-Ocaña, Barrientos, Bach and Wise2003). Similar results were found in another study on the wolf spider, P. prativaga (Jespersen and Toft, Reference Jespersen and Toft2003), which reported that with the weight of individuals increasing to 60% of that of the control individuals, complete growth recovery is likely to occur when individuals were subjected to various periods of restriction and re-feeding (Wang et al., Reference Wang, Cui, Yang and Cai2000; Tian and Qin, Reference Tian and Qin2003). In the present study, the weight of female spiders in the RF group had no significant change on days 7, 14, 21, and 28 compared to the CK group, which revealed that complete growth recovery occurred in female spiders.

Interestingly, compared to the CK group, the weight of adult male spiders in the RF group was not significantly recovered under re-feeding. This illustrated that there were significant gender differences in the growth recovery of P. pseudoannulata. Previous studies in other animal models have found that male roosters had a greater ability to show growth recovery compared to females (Shariatmadari and Torshizi, Reference Shariatmadari and Torshizi2004), and that in mice, males performed better than females in terms of weight gain rate and activity (Whitaker et al., Reference Whitaker, Totoki and Reyes2012). On the contrary, when measured over the entire period until maturation, only mosquitofish, Gambusia holbrooki, females showed growth recovery (Livingston et al., Reference Livingston, Kahn and Jennions2014), consistent with our results. Gender differences in growth recovery could be caused by differences in food consumption, the efficiency of converting food into body mass, digestive tract physiology, metabolic rate, or hormonal regulation (Livingston et al., Reference Livingston, Kahn and Jennions2014). We speculate that female P. pseudoannulata have higher reproductive costs than male spiders and need to grow faster by re-feeding growth. Further work is needed to determine the reason why P. pseudoannulata has gender differences in growth recovery.

In this study, dietary restriction or re-feeding growth had no significant effect on the mating success rate of P. pseudoannulata. Mating success may be influenced by mating intensity rather than by food restriction or growth recovery (Gibson and Uetz, Reference Gibson and Uetz2008). Female cannibalism during mating is determined by the degree of starvation, which may cause the female to attack the male as food (Zhang and Zhu, Reference Zhang and Zhu2012). Our results showed that the cannibalism rates of spiders in the RF and CK groups were lower than that in the RT group. It has been reported that food has an effect on cannibalistic behaviour, but does not affect the mating latency period and mating duration of spiders (Wilder and Rypstra, Reference Wilder and Rypstra2008). In our study, when environmental conditions were consistent, dietary restriction had no significant effect on the mating latency period and mating duration of spiders, consistent with previous studies.

The preoviposition period of laying eggs is related to the nutrient intake of spiders, and the preoviposition period of laying eggs is shorter for females with better nutrition (Wilder and Rypstra, Reference Wilder and Rypstra2008). In this study, the preoviposition period of the CK group with unlimited food was the shortest, followed by the RF group. This suggests that re-feeding for growth can shorten the preoviposition period of P. pseudoannulata. One previous study showed that there was no significant difference in fecundity between the fish, Aristichthys nobilis, under control and re-feeding conditions (Santiago et al., Reference Santiago, Gonzal, Aralar and Arcilla2004), consistent with our study. The incubation period and number of spiderlings of P. pseudoannulata was restored to normal levels by re-feeding for growth in our study. In some individuals, juveniles and adults feed on different resources and, while adult feeding is necessary for egg production, much of the nutrients allocated to the eggs come from juvenile feeding and cannot be completely recovered by adult feeding (Boggs, Reference Boggs1997; Fischer et al., Reference Fischer, O'brien and Boggs2004). The effects of juvenile food restriction on future reproductive success of female spiders were not due to reduced size, which was not affected by food treatment, and were also unlikely to be due to reduced storage reserves, as females acquire the majority, if not all, of the nutrients invested in eggs as adults (Boggs and Freeman, Reference Boggs and Freeman2005; Dmitriew and Rowe, Reference Dmitriew and Rowe2007). Therefore, the specific mechanism still needs to be further explored.

In this study, vitellogenin-related genes were shown to be expressed in P. pseudoannulata on different days following maturity. The relative expression levels of the Vg-3 gene were only significantly increased in the RT group compared to the CK and RF groups on day 7. It has been reported that juvenile hormones can induce the expression of Vg-1, Vg-2, and VgR-1, but do not affect the expression of Vg-3 (Yang et al., Reference Yang, Lu, Wu, Yu, Xu, Han and Liu2022); however, in the spiders, Parasteatoda tepidariorum, Vg expression was upregulated by 20-hydroxyecdysone (Bednarek et al., Reference Bednarek, Sawadro, Nicewicz and Babczyńska2019). In the case of restricted food, spiders gain more energy by increasing the time of moults to increase the instars (Zhu et al., Reference Zhu, Song, Chen, Yun, Zhang, Zhao and Peng2023), and 20-hydroxyecdysone is associated with the moulting of skin in juveniles (Drummond-Barbosa and Spradling, Reference Drummond-Barbosa and Spradling2001). We speculate that the expression levels of Vg-3 were affected by an increasing 20-hydroxyecdysone content under dietary restriction. Therefore, the potential mechanism through which juvenile food limitation could affect adult traits such as fecundity and longevity are through the epigenetic modification of gene expression (Pechenik, Reference Pechenik2006). The specific regulatory pathways still need to be further identified in starvation or growth recovery.

In conclusion, our results showed that dietary restriction can inhibit the growth and reproduction of spiders, and that re-feeding decreased cannibalism rates and increased the preoviposition period. In addition, dietary restriction also affected the expression of Vg-3 in P. pseudoannulata. Our results will contribute to the understanding of the impact of dietary restriction in predators of pest control, and provide a new perspective for the artificial rearing of spiders.

Supplementary material

The supplementary material for this article can be found at https://doi.org/10.1017/S0007485324000415.

Financial support

This study was supported by the National Natural Science Fund of China (31672317, 32302339); the Special Foundation for National Science and Technology Basic Research Program of China (2018FY100400); the Frontier Projects of the Applied Foundation of Wuhan Science and Technology Bureau (2019020701011464); and the Open Fund Project of Hubei Key Laboratory of Regional Development and Environmental Response [2022(B)003].

Competing interests

None.

Footnotes

*

These authors contributed equally to this work.

References

Austad, SN (1989) Life extension by dietary restriction in the bowl and doily spider, Frontinella pyramitela. Experimental Gerontology 24, 8392.CrossRefGoogle ScholarPubMed
Bednarek, AW, Sawadro, MK, Nicewicz, Ł and Babczyńska, AI (2019) Vitellogenins in the spider Parasteatoda tepidariorum – expression profile and putative hormonal regulation of vitellogenesis. BMC Developmental Biology 19, 119.CrossRefGoogle ScholarPubMed
Boggs, CL (1997) Dynamics of reproductive allocation from juvenile and adult feeding: radiotracer studies. Ecology 78, 192202.CrossRefGoogle Scholar
Boggs, CL and Freeman, KD (2005) Larval food limitation in butterflies: effects on adult resource allocation and fitness. Oecologia 144, 353361.CrossRefGoogle ScholarPubMed
Boggs, CL and Niitepõld, K (2016) Effects of larval dietary restriction on adult morphology, with implications for flight and life history. Entomologia Experimentalis et Applicata 159, 189196.CrossRefGoogle Scholar
Carey, JR, Liedo, P, Harshman, L, Zhang, Y, Müller, G-G, Partridge, L and Wang, JL (2002) Life history response of Mediterranean fruit flies to dietary restriction. Aging Cell 1, 140148.CrossRefGoogle ScholarPubMed
Chatzifotis, S, Papadaki, M, Despoti, S, Roufidou, C and Antonopoulou, E (2011) Effect of starvation and re-feeding on reproductive indices, body weight, plasma metabolites and oxidative enzymes of sea bass (Dicentrarchus labrax). Aquaculture 316, 5359.CrossRefGoogle Scholar
Cooper, TM, Mockett, RJ, Sohal, BH, Sohal, RS and Orr, WC (2004) Effect of caloric restriction on life span of the housefly, Musca domestica. The FASEB Journal 18, 15911593.CrossRefGoogle ScholarPubMed
Dai, M, Feng, P, Mao, T, Gu, H, Bian, D, Sun, H, Li, F, Wei, J and Li, B (2022) Study of compensatory growth based on different nutrition conditions of Bombyx mori. Journal of Asia-Pacific Entomology 25, 101948.CrossRefGoogle Scholar
Dmitriew, C and Rowe, L (2007) Effects of early resource limitation and compensatory growth on lifetime fitness in the ladybird beetle (Harmonia axyridis). Journal of Evolutionary Biology 20, 12981310.CrossRefGoogle ScholarPubMed
Drummond-Barbosa, D and Spradling, AC (2001) Stem cells and their progeny respond to nutritional changes during Drosophila oogenesis. Developmental Biology 231, 265278.CrossRefGoogle ScholarPubMed
Esperk, T and Tammaru, T (2010) Size compensation in moth larvae: attention to larval instars. Physiological Entomology 35, 222230.CrossRefGoogle Scholar
Fischer, K, O'brien, DM and Boggs, CL (2004) Allocation of larval and adult resources to reproduction in a fruit-feeding butterfly. Functional Ecology 18, 656663.CrossRefGoogle Scholar
Fu, D, Jing, L, Pan, Y, Zhu, J, Feng, X, Liu, M and Xiao, R (2022) Three heat shock protein genes and antioxidant enzymes protect Pardosa pseudoannulata (Araneae: Lycosidae) from high temperature stress. International Journal of Molecular Sciences 23, 12821.CrossRefGoogle ScholarPubMed
Gibson, JS and Uetz, GW (2008) Seismic communication and mate choice in wolf spiders: components of male seismic signals and mating success. Animal Behaviour 75, 12531262.CrossRefGoogle Scholar
Guedes, RNC, Smagghe, G, Stark, JD and Desneux, N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annual Review of Entomology 61, 4362.CrossRefGoogle ScholarPubMed
Hassanpour, M, Maghami, R, Rafiee-Dastjerdi, H, Golizadeh, A, Yazdanian, M and Enkegaard, A (2015) Predation activity of Chrysoperla carnea (Neuroptera: Chrysopidae) upon Aphis fabae (Hemiptera: Aphididae): effect of different hunger levels. Journal of Asia-Pacific Entomology 18, 297302.CrossRefGoogle Scholar
Hayward, RS, Noltie, DB and Wang, N (1997) Use of compensatory growth to double hybrid sunfish growth rates. Transactions of the American Fisheries Society 126, 316322.2.3.CO;2>CrossRefGoogle Scholar
Hector, KL and Nakagawa, S (2012) Quantitative analysis of compensatory and catch-up growth in diverse taxa. Journal of Animal Ecology 81, 583593.CrossRefGoogle ScholarPubMed
Huang, X, Quan, X, Wang, X, Yun, Y and Peng, Y (2018) Is the spider a good biological control agent for Plutella xylostella (Lepidoptera: Plutellidae)? Zoologia (Curitiba) 35, 18.CrossRefGoogle Scholar
Jespersen, LB and Toft, S (2003) Compensatory growth following early nutritional stress in the wolf spider Pardosa prativaga. Functional Ecology 17, 737746.CrossRefGoogle Scholar
Jiang, JC, Jaruga, E, Repnevskaya, MV and Jazwinski, SM (2000) An intervention resembling caloric restriction prolongs life span and retards aging in yeast. The FASEB Journal 14, 2135.CrossRefGoogle ScholarPubMed
Jobling, M and Johansen, SJS (1999) The lipostat, hyperphagia and catch-up growth. Aquaculture Research 30, 473478.CrossRefGoogle Scholar
Kasumovic, MM, Brooks, RC and Andrade, MCB (2009) Body condition but not dietary restriction prolongs lifespan in a semelparous capital breeder. Biology Letters 5, 636638.CrossRefGoogle ScholarPubMed
Kim, MK and Lovell, RT (1995) Effect of restricted feeding regimens on compensatory weight gain and body tissue changes in channel catfish Ictalurus punctatus in ponds. Aquaculture 135, 285293.CrossRefGoogle Scholar
Li, X, Li, W, Zhang, S, Sang, W, Peng, Y and Zhao, Y (2024) RNA interference against the putative insulin receptor substrate gene IRS1 affects growth and development in the pest natural enemy Pardosa pseudoannulata. Pest Management Science 80, 648660.CrossRefGoogle ScholarPubMed
Lichtenstein, JL, DiRienzo, N, Knutson, K, Kuo, C, Zhao, KC, Brittingham, HA, Geary, SE, Ministero, S, Rice, HK, David, Z, Scharf, I and Pruitt, JN (2016) Prolonged food restriction decreases body condition and reduces repeatability in personality traits in web-building spiders. Behavioral Ecology and Sociobiology 70, 17931803.CrossRefGoogle Scholar
Liu, L, Luo, M, Chen, F, Tan, W, Zhang, J and Li, X (2015) Study of the compensatory growth following starvation of juvenile golden pompano Trachinotus ovatus. Animal Husbandry and Feed Science 7, 178.Google Scholar
Livingston, JD, Kahn, AT and Jennions, MD (2014) Sex differences in compensatory and catch-up growth in the mosquitofish Gambusia holbrooki. Evolutionary Ecology 28, 687706.CrossRefGoogle Scholar
Lv, B, Wang, J, He, Y, Zeng, Z, Tang, YE, Li, N, Chen, L, Wang, Z and Song, QS (2021 a) Molecular response uncovers neurotoxicity of Pardosa pseudoannulata exposed to cadmium pressure. Environmental Pollution 280, 117000.CrossRefGoogle ScholarPubMed
Lv, B, Yang, HL, Wang, J, Zeng, Z, Li, N, Tang, YE, Wang, Z, and Song, QS (2021 b) Cadmium exposure alters expression of protective enzymes and protein processing genes in venom glands of the wolf spider Pardosa pseudoannulata. Environmental Pollution 268, 115847.CrossRefGoogle ScholarPubMed
Mair, W, Goymer, P, Pletcher, SD and Partridge, L (2003) Demography of dietary restriction and death in drosophila. Science 301, 17311733.CrossRefGoogle ScholarPubMed
McCue, MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 156, 118.CrossRefGoogle ScholarPubMed
Mehner, T and Wieser, W (1994) Energetics and metabolic correlates of starvation in juvenile perch (Perca fluviatilis). Journal of Fish Biology 45, 325333.CrossRefGoogle Scholar
Mitchell, RD III, Sonenshine, DE and Pérez de León, AA (2019) Vitellogenin receptor as a target for tick control: a mini-review. Frontiers in Physiology 10, 618.CrossRefGoogle ScholarPubMed
Moya-Laraño, J, Orta-Ocaña, JM, Barrientos, JA, Bach, C and Wise, DH (2003) Intriguing compensation by adult female spiders for food limitation experienced as juveniles. Oikos 101, 539548.CrossRefGoogle Scholar
Oerke, E (2006) Crop losses to pests. The Journal of Agricultural Science 144, 3143.CrossRefGoogle Scholar
Paul, AJ, Paul, JM and Smith, RL (1995) Compensatory growth in Alaska yellowfin sole, Pleuronectes asper, following food deprivation. Journal of Fish Biology 46, 442448.CrossRefGoogle Scholar
Paul, SC, Singh, P, Dennis, AB and Müller, C (2022) Intergenerational effects of early-life starvation on life history, consumption, and transcriptome of a holometabolous insect. The American Naturalist 199, 229E243.CrossRefGoogle ScholarPubMed
Pechenik, JA (2006) Larval experience and latent effects – metamorphosis is not a new beginning. Integrative and Comparative Biology 46, 323333.CrossRefGoogle Scholar
Pletcher, SD, Macdonald, SJ, Marguerie, R, Certa, U, Stearns, SC, Goldstein, DB and Partridge, L (2002) Genome-wide transcript profiles in aging and calorically restricted drosophila melanogaster. Current Biology 12, 712723.CrossRefGoogle ScholarPubMed
Preap, V, Zalucki, MP, Jahn, GC and Nesbitt, HJ (2001) Effectiveness of brown planthopper predators: population suppression by two species of spider, Pardosa pseudoannulata (Araneae, Lycosidae) and Araneus inustus (Araneae, Araneidae). Journal of Asia-Pacific Entomology 4, 187193.CrossRefGoogle Scholar
Qi, D, Yang, S, Li, H, Xia, M, Wang, T, Huang, Y and Chen, W (2016) Research progress on compensatory growth in animals. Chinese Journal of Animal Nutrition 28, 16551660.Google Scholar
Regalado, JM, Cortez, MB, Grubbs, J, Link, JA, van der Linden, A and Zhang, Y (2017) Increased food intake after starvation enhances sleep in Drosophila melanogaster. Journal of Genetics and Genomics 44, 319326.CrossRefGoogle ScholarPubMed
Santiago, CB, Gonzal, AC, Aralar, EV and Arcilla, RP (2004) Effect of stunting of juvenile bighead carp Aristichthys nobilis (Richardson) on compensatory growth and reproduction. Aquaculture Research 35, 836841.CrossRefGoogle Scholar
Schneider, WJ (1996) Vitellogenin receptors: oocyte-specific members of the low-density lipoprotein receptor supergene family. International Review of Cytology 166, 103137.CrossRefGoogle ScholarPubMed
Segoli, M, Lubin, Y and Harari, AR (2007) The effect of dietary restriction on the lifespan of males in a web-building spider. Evolutionary Ecology Research 9, 697704.Google Scholar
Shariatmadari, F and Torshizi, RV (2004) Feed restriction and compensatory growth in chicks: effects of breed, sex, initial body weight and level of feeding. British Poultry Science 45, 5253.CrossRefGoogle ScholarPubMed
Tian, X and Qin, JG (2003) A single phase of food deprivation provoked compensatory growth in barramundi Lates calcarifer. Aquaculture 224, 169179.CrossRefGoogle Scholar
Tufail, M and Takeda, M (2009) Insect vitellogenin/lipophorin receptors: molecular structures, role in oogenesis, and regulatory mechanisms. Journal of Insect Physiology 55, 88104.CrossRefGoogle ScholarPubMed
Wang, Y, Cui, Y, Yang, Y and Cai, F (2000) Compensatory growth in hybrid tilapia, Oreochromis mossambicus × O. niloticus, reared in seawater. Aquaculture 189, 101108.CrossRefGoogle Scholar
Wang, Z, Song, D and Zhu, M (2006) Functional response and searching behavior to the brown planthopper, Nilaparvata lugens by the wolf spider, Pardosa pseudoannulata under low dose chemical pesticides. Acta Entomologica Sinica 49, 295301.Google Scholar
Wang, Y, Kaftanoglu, O, Brent, CS, Page, RE Jr. and Amdam, GV (2016) Starvation stress during larval development facilitates an adaptive response in adult worker honey bees (Apis mellifera L.). Journal of Experimental Biology 219, 949959.CrossRefGoogle ScholarPubMed
Wang, J, He, Y, Peng, X, Wang, Z and Song, Q (2021) Characterization of cadmium-responsive transcription factors in wolf spider Pardosa pseudoannulata. Chemosphere 268, 129239.CrossRefGoogle ScholarPubMed
Weatherley, AH, Gill, HS and Casselman, JM (1987) The Biology of Fish Growth. London: Academic Press, p. 443.Google Scholar
Whitaker, KW, Totoki, K and Reyes, TM (2012) Metabolic adaptations to early life protein restriction differ by offspring sex and post-weaning diet in the mouse. Nutrition, Metabolism and Cardiovascular Diseases 22, 10671074.CrossRefGoogle ScholarPubMed
Wilder, SM and Rypstra, AL (2008) Diet quality affects mating behaviour and egg production in a wolf spider. Animal Behaviour 76, 439445.CrossRefGoogle Scholar
Xavier, B, Megarajan, S, Balla, V, Sadu, N, Ranjan, R, Babu, PS, Ghosh, S and Gopalakrishnan, A (2023) Impact of starvation and re-feeding on growth and metabolic responses of Indian pompano (Trachinotus mookalee) juveniles. Aquaculture 572, 739514.CrossRefGoogle Scholar
Yang, M, Wu, C, Qi, J, Hou, X and Yang, X (2007) Effects of nutritional restriction and compensatory growth on the mRNA expression level of insulin-like growth factor-1 (IGF-1) in Mongolian sheep. Journal of Inner Mongolia Agricultural University 28, 912.Google Scholar
Yang, H, Peng, Y, Tian, J, Wang, J, Wei, B, Xie, C and Wang, Z (2018) Rice field spiders in China: a review of the literature. Journal of Economic Entomology 111, 5364.CrossRefGoogle Scholar
Yang, T, Song, X, Xu, X, Zhou, C and Shi, A (2021) A comparative analysis of spider prey spectra analyzed through the next-generation sequencing of individual and mixed DNA samples. Ecology and Evolution 11, 1544415454.CrossRefGoogle ScholarPubMed
Yang, ZM, Lu, TY, Wu, Y, Yu, N, Xu, GM, Han, QQ and Liu, ZW (2022) The importance of vitellogenin receptors in the oviposition of the pond wolf spider, Pardosa pseudoannulata. Insect Science 29, 443452.CrossRefGoogle ScholarPubMed
Yip, EC and Lubin, Y (2016) Effects of diet restriction on life history in a sexually cannibalistic spider. Biological Journal of the Linnean Society 118, 410420.CrossRefGoogle Scholar
Yip, EC, Levy, T and Lubin, Y (2017) Bad neighbors: hunger and dominance drive spacing and position in an orb-weaving spider colony. Behavioral Ecology and Sociobiology 71, 111.CrossRefGoogle Scholar
Zhang, J and Zhu, L (2012) Advances in research on reproduction behavior of spiders. Acta Arachnologica Sinica 21, 6164.Google Scholar
Zhang, H, Wen, L, Li, Z and Li, C (2023) Economic web-building behavior and behavioral investments trade-offs in a cobweb spider. Frontiers in Ecology and Evolution 11, 1164310.CrossRefGoogle Scholar
Zhu, Y, Song, L, Chen, L, Yun, Y, Zhang, W, Zhao, Y and Peng, Y (2023) Energy allocation of the wolf spider Pardosa pseudoannulata under dietary restriction. Insects 14, 579.CrossRefGoogle ScholarPubMed
Figure 0

Figure 1. Biological characteristic parameters of spiderling P. pseudoannulata: (a) carapace length, (b) carapace width, and (c) weight. The data are shown as mean ± standard error and are used to analyse by two-factor repeated measures analysis of variance (ANOVA).

Figure 1

Figure 2. Weight of adult P. pseudoannulata. (a) weight of female, (b) weight of male. The data are shown as mean ± standard error and are used to analyse by two-factor repeated measures analysis of variance (ANOVA).

Figure 2

Figure 3. Mating success rates and cannibalism rates of adult P. pseudoannulata. The data are shown as mean ± standard error. The different lowercase letters indicate significant differences among each group.

Figure 3

Figure 4. Reproduction parameters of P. pseudoannulata: (a) mating latency period, (b) mating duration, (c) preoviposition period, (d) egg stage, and (e) number of spiderlings. The data are shown as mean ± standard error. The different lowercase letters indicate significant differences among each group.

Figure 4

Figure 5. Relative expression levels of the VgR-1 and Vg genes of P. pseudoannulata in each group after maturation. The data are shown as mean ± standard error. The different lowercase letters indicate significant differences among each group.

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