Are female Pardosa spiders (Araneae: Lycosidae) from a Mexican coffee crop more efficient than males in capturing a standard prey of various sizes?

doi:10.21203/rs.3.rs-4682875/v1

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Are female Pardosa spiders (Araneae: Lycosidae) from a Mexican coffee crop more efficient than males in capturing a standard prey of various sizes?

https://doi.org/10.21203/rs.3.rs-4682875/v1

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Wolf spiders (Lycosidae) are considered one of the main groups of predators in economically relevant crops. Despite their importance, most studies have focused on Nearctic species and have aimed to determining diet composition and analyzing predation primarily using female spiders as models. Although it is known that male spiders also hunt and consume prey effectively, the type and quantity of prey consumed by males may, due to sexual dimorphism, complement that of females. There is an evident lack of information regarding to males which limits their knowledge as potential biological control agents. The study aimed to experimentally assess prey acceptance, immobilization time, and the length of predatory behavior in both female and male Pardosa spiders when exposed to a standard prey (Acheta domesticus) of different sizes. Our findings revealed no significant differences between females and males in terms of prey acceptance, immobilization time, or length of predatory behavior. The increase in relative prey size was related to a decrease in prey acceptance by the spiders. Furthermore, prey immobilization time and length of predatory behavioral sequences increased in relation to increasing prey size. Our findings support the idea that both female and male Pardosa spiders are voracious predators with similar trophic attributes. Size emerges as a critical factor in prey selection by these generalist predators. Understanding the preferred prey size range can be useful for selecting beneficial controllers in various crops.

spiders

trophic ecology

predation

prey size

agroecosystems

Maintaining natural predators in crops plays a central role in agroecological strategies, as a high density and diversity of these organisms can promote pest regulation (Altieri 2002; Michalko et al. 2019a), thereby reducing the use of pesticides that adversely affect human health and ecosystems. Despite the high diversity of spiders and other predators within agroecosystems (Birkhofer et al. 2013), only a few species contribute the majority of biological control due to their high abundance (agrobiont species). Understanding the trophic attributes of these agrobiont species is therefore valuable for pest management strategies (Michalko and Pekár 2015). Lycosidae spiders are among the most dominant predators in globally important agroecosystems such as maize (Midega et al. 2008), wheat (Kerzicnik et al. 2013), citrus (Maqsood et al. 2016), and coffee (Marín et al. 2016). They are present throughout most agricultural cycles (Quijano-Cuervo et al. 2024) and have the capacity to consume a wide variety of prey (Kielty et al. 1999; Lang et al. 1999; Schmidt et al. 2012; Saqib et al. 2022). Experimental evidence indicates that Lycosidae species exhibit high predation rates and employ multiple behavioral strategies against different insects, including agriculturally significant pests such as lepidopterans (Spodoptera frugiperda, Helicoverpa armigera), bugs (Piezodorus guildinii), dipterans (Drosophila, Anastrepha species), and crickets (Nyffeler and Sunderland 2003; Rendon et al. 2016; García et al. 2021, 2022). The dominance and high predatory capacity of Lycosidae spiders in crops underscore their importance and highlight the need for more studies.

Experimental studies on the predatory behavior of spiders are essential to understand their efficacy in pest control and their impact on agriculture (García et al. 2021). However, most research has been limited to specific regions such as Europe (Nyffeler and Benz, 1988; Nyffeler and Sunderland, 2003) and has primarily focused on determining the diet and analyzing the predatory behavior of species using mainly female spiders as study models (Nentwig and Wissel 1986; Nyffeler et al. 1987). This focus on females is due to their greater voracity and higher hunting effectiveness compared to males (Schoener 1971; Pekár et al. 2011). Additionally, most web-building spiders males (e.g. Araneidae) stop hunting upon reaching sexual maturity due to loss of web-building ability (Foelix 2011), which might explain why males are not considered as good models for the study of predation. Nevertheless, evidence suggests that male spiders from different guilds can also effectively hunt and consume prey (Kielty et al. 1999; Sherawat and Butt 2014) and due to intersexual differences in size, morphology, and activity patterns, the type of prey consumed by male spiders may complement in size and developmental stages to those consumed by females (Walker and Rypstra 2002; Pekár et al. 2011; García et al. 2022).

Males of wolf spiders (Lycosidae) are known to effectively capture and consume prey (Charnov 1978; Walker and Rypstra 2002). However, due to ecological and behavioral differences, Lycosidae males typically capture smaller and fewer prey compared to females (Nyffeler and Benz 1988; Walker and Rypstra 2002). For instance, Walker and Rypstra (2002) demonstrated that in two species, Hogna helluo and Pardosa milvina, males captured and consumed fewer prey than females. Additionally, this study found that males had longer prey immobilization times and were more likely to capture smaller prey. The higher consumption rate by females may be attributed to greater energy demands associated with reproductive roles (Pekár et al. 2011). Furthermore, female Lycosidae axhibit higher capture effectiveness (e.g. shorter immobilization times), as a result of more developed hunting organs like chelicerae and a higher amount and concentration of venom (Walker and Rypstra 2001). However, in species such as Lycosa thorelli and Pavocosa sp., prey acceptance probability is similar between sexes and not affected by predator size (García et al. 2021), suggesting that females are not universally more voracious or effective hunters than males. Despite the importance of analyzing intersexual differences among crop-associated predators, our understanding of spiders remains limited (Benamú et al. 2017; Pekár et al. 2017).

Size is a critical parameter influencing the trophic niche of predators (Nentwig 1987; Shine 1989, 1991; Michalko et al. 2019b). Trophic differences between the sexes of spiders may not only be related to the quantity of prey consumed, but also to the variability in prey capture depending on size (Nentwig 1987). Non-web-hunting spiders such as Lycosidae typically target prey smaller than themselves (ranging between 50% and 80% of the spider's size) (Nentwig and Wissel 1986). However females, known to consume larger quantities of prey (Walker and Rypstra 2002), are likely to target and consume larger prey to maximize nutritional rewards useful for egg development and rearing (Nentwig and Wissel 1986; Pekár et al. 2011; García et al. 2021). Conversely, males may prioritize their hunting efforts on smaller prey, investing more energy in mate searching (Pekár et al. 2011). To effectively capture larger prey, spiders must possess morphological traits that enable efficient hunting with minimal energy expenditure and reduced risk of injury (e.g. larger chelicerae and more venom in females, Walker and Rypstra 2001; Pekár et al. 2011). In addition to morphological characteristics, spiders are expected to frequently evaluate the risk associated with attacking prey that could potentially harm them through combat (Riechert and Łuczak 1982), which likely influences their predatory behavior as prey size increases (García et al. 2021).

Given the potential of agrobiont spiders of the Lycosidae family as effective predators of numerous crop insects (Nyffeler and Sunderland 2003), the study aimed to experimentally assess prey acceptance, immobilization time, and the length of predatory behavior among female and male Pardosa spiders when exposed to varying sizes of a standard prey (Acheta domesticus). We hypothesize that increasing the size of the cricket would reduce prey acceptance rates by spiders and prolong immobilization times and the length of predatory behavior, particularly among males compared to females. Considering that knowledge of intersexual differences is relevant in biological control programs, we expect these results to serve as a baseline for further studies that explore additional aspects, including the role of males as natural enemies in crops.

Study area and species

Pardosa individuals were collected from a shaded coffee plantation located in Teocelo, Veracruz, Mexico (96°58'19.837" W, 19°23'10.502" N; 1,050 masl). The average annual temperature in the area is 18.4°C, with an annual precipitation of 1,797 mm. We manually captured 100 adult individuals, consisting of 50 females and 50 males (Figure 1A-B). The spiders were individually housed in 118 cm³ terrariums, which were maintained in the laboratory of the Instituto de Neuroetología, Universidad Veracruzana, for a one-month observation period prior to the experiment. To minimize stress, the spiders were provided with a substrate similar to their natural environment, along with water (ad libitum) and live food twice a week (Anastrepha ludens and Drosophila melanogaster). Females carrying egg sacs and/or recently hatched spiderlings were excluded to prevent interference with their hunting performance (Edgar 1969; Moring and Stewart 1992). No approval of research ethics committees was required to accomplish the goals of this study because experimental work was conducted with an unregulated invertebrate species.

Experimental design

Five days before starting the experiments to evaluate the predator behavior, we standardized the hunger levels of spiders by feeding them to satiation with flies (Anastrepha ludens and Drosophila melanogaster). For the experiments, we used farm-reared crickets (Acheta domesticus) as prey, which have been used in previous studies as a prey model (Eggs et al. 2015). Crickets were randomly offered to the spiders, aiming to provide different sizes of prey, in a gradient of smaller to larger relative to each spider's size. A total of 45 individuals of each sex were used, and 270 A. domesticus individuals were included in the experiment (cricket size: min = 0.31 mm, mean = 0.69 mm, max = 1.24 mm). Each spider participated in three independent trails. After the first trial, each spider was fasted for five days before repeating the experiment. If a spider did not feed during a trial, a small fly was offered until feeding occurred. The experimental arena consisted of a 10 cm diameter plastic Petri dish divided in half by a removable opaque barrier. Each female or male spider was randomly placed on one side of the arena, and the cricket was introduced on the opposite side. After a one-minute acclimatization, the experiment began by removing the barrier. The trial ended when the cricket was captured, or after 10 minutes if it was not captured. We recorded the trials using an overhead video camera (Canon Vixia HFR42) placed 40 cm above the arena on a tripod (see Online Resource 1; supplementary video). These videos were used for subsequent analysis and to obtain additional data.

Variables and data analysis

Measurements of spiders and prey were taken from images obtained from the videos using ImageJ software. The total size of the spiders was measured from the length of the prosoma to the opisthosoma, excluding the legs, while the size of the crickets was measured from the head to the abdomen, excluding the legs and antennae. Prey acceptance was evaluated based on whether the spiders consumed or rejected the prey. Rejection was defined as spiders not biting or consuming the crickets after 10 minutes of contact. Capture efficiency was evaluated by latency, defined as the time between the first bite and total immobilization of the prey. This time was measured from the analysis of videos of spiders that accepted prey of different sizes (42 females and 19 males). Additionally, predatory behavior was defined from the video analysis, establishing the behavioral sequence through six types: orient, approach, assault, hold and bite (Figure 1C, Table 1). For individuals, the frequency of occurrence of each behavioral pattern was measured, and the total length of the predatory behavior of each spider was obtained. The types of behavior were defined based on previous studies (García et al. 2021) and the analysis of behavior through the videos was done in Boris software (Friard and Gamba 2016).

Table 1. Ethogram of predatory behaviors observed in Pardosa spiders that accepted prey.

Behavior	Description	Female (# of behavioral sequences)	Male (# of behavioral sequences)
Orient	The spider orients itself with the prosoma in the direction of the prey.	30	10
Approach	The spider moves towards the prey by running or walking.	119	33
Assault	The spider propels itself in the direction of the prey with its hind legs.	17	4
Hold	The spider holds the prey with the first two pairs of legs.	76	27
Bite	The spider bites the prey with its chelicerae.	78	28

Using linear models, we analyzed whether the total size of the spiders differed between sexes. Additionally, using Generalized Linear Mixed Models (GLMMs), we evaluated whether prey acceptance, latency (i.e., immobilization time), and the length of behavioral sequences (only for spiders that accepted prey) were affected by the sex of the spiders and the size ratio between the spiders and the cricket prey (spider size/cricket size). We constructed GLMMs with a binomial distribution for prey acceptance (acceptance= 1, rejection= 0), and a negative binomial distribution for latency (time in seconds) and behavior length (sum of the frequencies of behavioral transitions). Individual spiders were included as a random factor in the GLMMs due to the three repeated measures for each spider. We ensured that all models met the assumptions of normality, homoscedasticity, and checked for overdispersion in models with negative binomial errors. To construct the models, we used the glm, glmer and glmer.nb functions from the lme4 package in R software (R Core Team 2022).

We found sexual dimorphism in the size of Pardosa individuals, with female spiders being on average larger than males (females = 5.6 mm [0.55–0.58 CI], males = 4.0 mm [0.39–0.42 CI]; X²_df=1 = 289.01, p < 0.001). Out of all the individuals used in the experiment, 42 females (59 attacks) and 19 males (19 attacks) accepted at least one of the three preys items offered during the experiments.

The probability of cricket acceptance, immobilization time, and the length of predatory behavior sequences by Pardosa spiders did not vary significantly between sexes. For spiders of both sexes, the probability of prey acceptance significantly decreased with an increase in the size ratio of the crickets (β = -7.07, X²_df=1 = 36.0, p < 0.001; Fig. 2A), while immobilization time (β = 2.01; X²_df=1 = 35.3, p < 0.001; Fig. 2B) and the length of predatory behavior (β = 0.96; X²_df=1 = 7.35, p = 0.006; Fig. 2C) significantly increased with prey size.

In this study, we experimentally investigated intersexual variation in the trophic ecology of a euryphagous predator from the genus Pardosa (Lycosidae) (Zhong et al. 2019), a spider group that significantly dominates agroecosystems worldwide (Birkhofer et al. 2013). Contrary to our expectations, we did not find significant differences in the probability of prey acceptance, immobilization time, and predatory behavior length between female and male Pardosa spiders. Individuals of both sexes similarly decreased their probability of prey acceptance as the relative size of the crickets increased, while prey immobilization time and the length of predatory behavior increased with cricket size.

We observed that the probability of prey acceptance by Pardosa spiders did not significantly differ between female and male individuals. This finding aligns with previous studies conducted on two Lycosidae species (L. thorelli and Pavocosa sp), where García et al. (2022) found that individuals of different sexes consumed S. frugiperda larvae of different sizes with equal probability. Like other species previously studied (H. helluo and P. milvina), the Pardosa species exhibits marked sexual dimorphism, characterized by larger females (Walker and Rypstra 2002). However, male Pardosa hunted prey of similar size to females with equal probability, suggesting that intersexual niche divergence may not be a generalizable pattern across all spider species (García et al. 2022). For our study species, as with most spiders (Walker and Rypstra 2001, 2002; Pekár et al. 2011), intersexual divergence in trophic niche may manifest in the quantity of prey consumed. This is supported by the fact that 42 females attacked 59 of the offered crickets, while only 19 males participated in 19 attacks. The observation that female and male spiders in crops attack and consume prey within a similar size range suggests dietary redundancy between sexes, potentially accessing similar cohorts or types of prey, which could have significant implications for biological control (Nyffeler and Benz 1988; Rendon et al. 2016; García et al. 2022). For example, the overexploitation of certain pest cohorts at specific times in agricultural cycles can contribute to effective control of herbivore populations that affect crop yields (Michalko et al. 2019b).

Similar to cricket acceptance, prey immobilization time by spiders did not significantly differ between sexes. It has been previously suggested that the larger body size of females, as well as the greater development of hunting organs such as chelicerae, and higher venom quantity and concentration, contribute to higher hunting effectiveness of females, expressed in a shorter latency time (immobilization) (Walker and Rypstra 2002). However, contrary to previous evidence, we demonstrated that males of the Pardosa species are just as efficient in handling and immobilizing prey as females, indicating that their venom potentially has a similar effect on the crickets used in this study. Valenzuela et al. (2019) demonstrated that males of a wandering spider (Phoneutria boliviensis) have venom even more efficient than that of females. Regardless of sex, prey immobilization time increased exponentially with the relative size of the crickets, just as the probability of prey acceptance decreased with prey size. This likely indicates the limits of the trophic niche of the Pardosa species studied, which may be related to prey of a smaller or on-average similar size to the spider, common for generalist predators (Foelix 2011). However, it is necessary to consider that, although various species of orthopterans are associated with coffee plantations and other crops (e.g. Sphenarium purpurascens, Cerritos and Cano-Santana 2008), the prey we used as a model (A. domestica) is not native to the spider's habitat (crops). It is likely that using prey such as dipterans or larvae of lepidopterans and beetles occurring in coffee plantations (Segura et al. 2004; Dantas et al. 2021; Góngora et al. 2023), the effectiveness of the spider's venom and its relationship with prey size would be different (García et al. 2021, 2022). Spider species can have variable efficacy depending on the type of prey they access; therefore, further research is needed to understand the biological bases mediating predator-prey interactions associated with crops. Although several studies suggest the possibility of a similar efficiency in the predatory behavior and efficiency between males and females, further studies should explore the reproductive condition of females, as this might be more voracious and aggressive before oviposition as it has been shown in other predators (Cabral et al. 2009).

Finally, we observed that the length of predatory behavior in spiders increased with the size of the crickets. García et al. (2022) similarly demonstrated that a relative increase in prey size causes an increase in the sequences of predatory behavior in spiders. Consuming larger prey involves a high energetic cost for spiders, requiring a greater number of movements before biting and completely paralyzing the prey (Griffiths 1980; García et al. 2021). In this case, Pardosa spiders exhibited a greater number of “cautious” behaviors, approaching larger prey more frequently, and holding and biting the prey more times. This higher number of approaches, holds, and bites is associated with events where larger prey managed to escape and the spiders had to recapture them, or when spiders wanted to inoculate more venom to achieve effective capture (Riechert and Łuczak 1982). Accessing prey at least 1.5 times larger than the spiders involves a high energetic cost, suggesting that niche divergence between the sexes of Pardosa spiders may be in terms of the quantity of prey they hunt, with female spiders maximizing their energy intake by consuming more prey (Walker and Rypstra 2002; Walker and Irwin 2006). This finding suggests that efficiency in prey capture and optimization of consumed energy are crucial factors in Pardosa hunting strategies, with potential implications for their role in biological control within agroecosystems.

Our study provides experimental evidence that a species of Pardosa found in Mexican coffee crops effectively preys and consumes A. domesticus, a widely studied standard prey. Both female and male individuals of this Pardosa species demonstrate a preference for prey of sizes similar to their own. However, this preference may not apply universally to all prey species found in crops, highlighting the need for additional experimental investigation. Size clearly emerges as an important factor influencing prey selection among spiders. Understanding the preferred size range of prey by generalist predators such as spiders can significantly assist in selecting potentially beneficial species for various crop types, aiming to effectively control harmful herbivores. Considering that males and females show a similar efficiency regarding prey capture and based on additional evidence further studies should compare the trophic ecology of males and females in different spider group, particularly in web and non-web-building spiders.

Conflict of interest statement

The authors declare no conflicts of interest.

Data availability

The datasets are available from the corresponding author on reasonable request.

Acknowledgments

The development of this project was possible thanks to the support of the Instituto de Neuroetología of the Universidad Veracruzana, we also thank Mr. Luis Donato Pale Tlapa for allowing us to collect the Pardosa spiders.

Author contributions

Luis G. Quijano-Cuervo: Conceptualization; formal analysis; visualization; writing – original draft. Mauricio Olvera Pale: Conceptualization; experimentation. Luis F. García Hernández: Conceptualization; supervision; writing. Dulce Rodríguez-Morales: Conceptualization; experimentation; supervision; writing – original draft.

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No competing interests reported.

supplementaryvideo.mp4
Supplementary information Video 1. In the video it is possible to observe how the predation behavior of the Pardosa spider occurs, from when it identifies and orients itself towards the prey, it approaches the prey, captures it and bites it.

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30 Jul, 2024
Editor assigned by journal
30 Jul, 2024
Submission checks completed at journal
26 Jul, 2024
First submitted to journal
03 Jul, 2024

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Are female Pardosa spiders (Araneae: Lycosidae) from a Mexican coffee crop more efficient than males in capturing a standard prey of various sizes?

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Abstract

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Introduction

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Discussion

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Status:

Version 1