Next Article in Journal
Two New Species of Crayfish of the Genus Cherax (Crustacea, Decapoda, Parastacidae) from Western and Eastern Indonesian New Guinea
Previous Article in Journal
New Cases of Teratology, Albinism, Abnormal Pigmentation, Gynandromorphism, and Injury Healing in Scorpions (Arachnida: Scorpiones)
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Arthropoda
Volume 2
Issue 4
10.3390/arthropoda2040018
arthropoda-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Prevalence of Egg Parasitoids of Two Cobweb Spiders in a Tropical Urban Gradient

by
Natalia Jiménez-Conejo
1,2,3,*,
Paul E. Hanson
1,2,
Eduardo Chacón-Madrigal
1,2 and
Geovanna Rojas-Malavasi
1,2
1
Escuela de Biología, Universidad de Costa Rica, San José 11503, Costa Rica
2
Centro de Investigación en Biodiversidad y Ecología Tropical, Universidad de Costa Rica, San José 11503, Costa Rica
3
Centro de Investigación en Ciencias del Mar y Limnología, Universidad de Costa Rica, San José 11503, Costa Rica
*
Author to whom correspondence should be addressed.
Arthropoda 2024, 2(4), 250-263; https://doi.org/10.3390/arthropoda2040018
Submission received: 22 September 2024 / Revised: 18 November 2024 / Accepted: 20 November 2024 / Published: 27 November 2024
Browse Figures
Review Reports Versions Notes

Abstract

:
Parasitoidism strongly influences the structure of the spiders’ populations, and it can be affected by environmental factors such as those caused by anthropogenic actions. We studied the prevalence of parasitoids in egg sacs and the proportion of eggs parasitized in each egg sac of two synanthropic spider species, one native to the American continent (Parasteatoda tepidariorum) and another recently introduced to the Americas (Latrodectus geometricus). We conducted the study at two scales, along an urban gradient (from highly urbanized to rural sites) and in the vegetation surrounding each sampling site (microscale). We expected to find a larger prevalence of parasitoids in the most urbanized sites and around sampling sites with more vegetation. However, we saw more parasitized egg sacs at the intermediate urbanized site for both species, and the vegetation surrounding the sampling sites did not affect the number of parasitized egg sacs. Therefore, conditions in the site with intermediate urban development favored parasitoids. We also found more parasitized egg sacs in P. tepidariorum than in L. geometricus, which is likely a consequence of native parasites not being adapted to a new host. The proportion of eggs parasitized was similar for both species in all sites, which may be related to the behavior (e.g., searching behavior) and number of spider eggs a female parasitoid can parasitize.

1. Introduction

Parasitoids impact the host population similar to the way predators do because they kill the host [1,2]. Therefore, parasitoids affect the host’s demography, behavior, ecology, and evolution [2]. Spiders are affected by several parasitoid insects, mainly in the order Hymenoptera and Diptera [1]. Over 1000 parasitoids, specialists, or generalists [3], use ground-dwelling and web-building spiders as hosts [1,2]. Some spider parasitoids are endoparasitoids in eggs, and it is suggested that this interaction is responsible for the diversification of egg sacs in spiders [4]. Spider egg sacs are usually exposed to the environment, which could affect the spiders’ development, and/or that of the parasitoids [5]. As adults, parasitoids have a different feeding strategy; they are free-living and feed primarily on nectar and honeydew [6]. Consequently, their abundance depends on both the habitat of the host as well as host’s abundance [1].
Urbanscapes provide new habitats for some invasive and tolerant native species, whose populations often increase rapidly [7,8,9,10,11,12,13,14,15]. As the populations of these species grow, the antagonistic interactions, such as predation and parasitism, may change among some urban species [9,14]. For instance, the abundance of some parasites and predators increases because urban conditions provide new resources and reduce the composition and abundance of their natural enemies [11,16], so parasites and predators can affect the reproduction of some host and prey species [11,17].
Research on the effects of urbanization on spiders has primarily focused on the spiders themselves [18], and very little is known about the impact on the antagonistic interactions between spiders and other arthropods, particularly host-parasite interactions [19,20,21,22]. The eggs of two synanthropic spider species, Latrodectus geometricus Koch, 1841 and Parasteatoda tepidariorum Koch, 1841, are parasitized by wasps, especially Baeus spp. Haliday, 1839 [23,24,25,26]. More recently, it was found that increasing urbanization had little impact on the presence of parasitoids in the eggs of L. geometricus [19,20,21,22]. However, information on how urbanization affects egg parasitoid prevalence in spiders is still incomplete.
In this study, we investigated the prevalence of predation and parasitism on eggs of two synanthropic cobweb spiders (Theridiidae Sundevall, 1833), P. tepidariorum and L. geometricus, at two different scales, regional and local. For the regional scale, we selected three sites with varying degrees of urbanization, and for the local scale, we estimated the proportion of green area surrounding the collecting sites. Previous studies reported that the prevalence of parasitoids in egg sacs of P. tepidariorum increased as urbanization progressed [23,26]. Based on these findings, we predicted that the number of egg sacs attacked by parasitoids or egg predators, and the proportion of parasitized eggs per egg sac, would increase with urbanization for both spider species since some of the changes in the urban environment presumably favor the parasitoids [16,27]. We also predicted a greater prevalence of parasitoids in sites with a greater proportion of vegetation (green area) since vegetation may provide resources (e.g., nectar for adult parasitoids) and favorable environmental conditions for parasitoids [28]. Finally, given that L. geometricus is a recent invader of the Americas [29,30] whereas P. tepidariorum is a native species [31], we expected higher parasitism in the native species (P. tepidariorum) than in the invasive species (L. geometricus), since native parasites usually require some time to adapt to and attack new hosts [32,33].

2. Materials and Methods

2.1. Study Species

Parasteatoda tepidariorum (Theridiidae) is a common cosmopolitan synanthropic species that builds solitary webs on plants and buildings [34,35]. Its origin is hypothesized to be Neotropical [31,36]. Latrodectus geometricus (Theridiidae) is a native species in Southern Africa or the Mediterranean region that has invaded the Americas [22,29,37] (Figure 1). After arriving, this species rapidly expanded its distribution over nearly the whole American continent [29,31,37]. In Costa Rica, L. geometricus was first observed in the 1990s but became frequent in urbanized areas after 2010 [38], and a previous report [26] conducted in one of the urban locations included in the present study did not find egg parasitoids in this species. However, there are some reports of egg parasitoids found in L. geometricus in North and South America [19,20,21,22,39,40,41].

2.2. Study Site

All sampling sites were located in the western section of the Costa Rican Central Valley (Figure 2) at an elevation of 1200 m, with an average temperature of 20.5 °C, with a dry season from December to April. We selected three sites based on the urban buildings and green zones (Figure 3, Table S1). The Central Campus of the University of Costa Rica, San José province (9°54′ N, 84°03′ W) was considered the most urbanized site since it includes many large buildings with only some green patches, gardens (dominated by grass), and small remnant patches of second-growth forest [6] (Figure 2). The Occidental Campus of the University of Costa Rica, Alajuela province (10°08′ N, 84°47′ W) was considered as the site with intermediate urbanization. This campus includes buildings separated by large green areas with abundant trees and grasslands. The third study site was Concepción, San Ramón, Alajuela province (10°11′ N, 84°44′ W). It is a small village in the countryside, dominated by coffee plantations, patches of trees, and second-growth forests. At this site, some farmers apply pesticides once or twice a year, but there are also green agriculture sites free of pesticides.
To define the urban categorizations at the macroscale level, we estimated the percentage of green area vs. the gray area in a buffer zone of 2.5 km around each sampling site, using the polygon selection tool in the QGIS software and images from Google Earth for the year of sampling (version 3.22, QGIS.ORG, Böschacherstrasse, Switzerland) [42]. The green areas consisted of gardens, secondary forests, and patches of early-growth vegetation; the light green color represents agricultural patches. The gray areas included human-made constructions such as buildings, houses, streets, and sidewalks. The dispersion capability and ecological requirements of egg parasitoids of spiders are poorly known; therefore, we did not have a good biological criterium that could be used to define a buffer zone. Considering the small size of the parasitoids and the fact that female Baeus species are apterous [24,25,43]), we arbitrarily selected 2.5 km as the potential area that could affect the biology (e.g., dispersion, reproduction) of the parasitoids (Figure 3, Table S1).
Within each study site (2.5 km buffer zone), we sampled different groups of buildings; 9 buildings corresponding to the site categorized as highly urbanized, 8 buildings in the site with intermediate urbanization, and only 3 houses associated with the site corresponding to low urbanization. We only sampled three houses at the site with low urbanization because, in this rural site, the occupants frequently cleaned the walls. To avoid bias in the study, only three houses were sampled where the walls were not disturbed during the sampling period. Also, the sampling in these houses was conducted at least once a month during the study period (ten months).
At each group of buildings, we estimated the percentage of green vs. gray areas to evaluate their effect on parasitoids at the local scale (microscale). To calculate the rate of green area, we took a panoramic photo at 10 m in front of each sampling structure (i.e., buildings and houses, Figure 4). From each photo, we obtained the proportion of bare soil, green area (e.g., grass and shrubs-trees), cemented area, and number of trees and bushes in front of each building using the polygon selection tool in Image J (version 1.53j, National Institutes of Health and Laboratory for Optical and Computational Instrumentation, Wisconsin, USA) [44]. We considered the local scale (microscale) component important because the surrounding environment could influence prey abundance for spiders, as well as the environmental conditions (e.g., relative humidity and ambient temperature) for spiders and parasitoids. These variables were measured once, as the number of trees, bushes, and cemented areas remained constant throughout the year.
We combined the local scale variables (number of trees, percentage of grass and bushes, and percentage of cemented area) using a principal component analysis (PC) because we did not have evidence for which variables (or combination of variables) directly affect the biology of spiders and parasitoids. From this analysis, we used the first PC (PC1) that explained 86% of the variance of local scale variables for P. tepidariorum and 74% for L. geometricus. For P. tepidariorum, PC1 correlates positively with grass (0.95), number of bushes (0.95), and trees (0.87) and negatively with cemented (−0.95) and bare soil areas (−0.22). For L. geometricus PC1 correlates positively with grass (0.89), number of bushes (0.83), and trees (0.89) and negatively with cemented area (−0.89); thus, PC1 represents the vegetation cover around the collecting sites for both spider species. The PC scores characterized the immediate environment around each group of buildings. However, to evaluate the effect of the immediate environment on the prevalence of parasitoids at each urban location rather than at each group of buildings, we included the buildings as a random factor in the models (see Data Analyses section).

2.3. Data Collection

We conducted nine samplings during the dry season (January–April) and ten during the rainy season (May–October) in 2017. During the study period, we collected 161 egg sacs from A. tepidariorum (83 in the dry season and 78 in the rainy season) and 141 from L. geometricus (81 in the dry season and 60 in the rainy season). We manually collected one egg sac from each web of A. tepidariorum and L. geometricus found on the external walls of buildings and houses for a minimum area of 10 m2 (2 × 5 m) per sampling in each site. After collecting the egg sacs, we verified that spiders remained in their webs so that the density of adult females was not artificially affected in the study sites. During each sampling, we measured the area of the walls sampled. Because some buildings were painted or cleaned during the sampling period, we collected spider egg sacs from another unaffected building in the same area which did not affect the immediate landscape variable we measured.
We placed each egg sac in a plastic container (6 × 3 cm) at room temperature (~22 °C) and checked each one every two days for the emergence of parasitoids, egg predators, or spiderlings. We collected all parasitoids, predators, and spiderlings from each egg sac. After most parasitoids and spiderlings had emerged, we checked the egg sacs for two additional weeks to count individuals that emerged asynchronously. Following [26], we opened each egg sac to count unhatched spider eggs (brownish eggs with chorion collapsed, rather than whitish eggs with smooth chorion) and parasitized eggs (blackish eggs with a parasitoid pupa) that had incomplete development, as well as spiderlings, parasitoids, and predators that had failed to exit the egg sacs. We quantified the number of eggs parasitized and not parasitized in each egg sac collected for each species during each sampling event at each site.
With these data, we obtained the number of egg sacs attacked by parasitoids and egg predators. We also calculated the proportion of eggs within each egg sac attacked by parasitoids, dividing the number of emerged and unemerged parasitoids by the total number of eggs in the egg sac. The total included the following: the number of parasitoids, number of spiderlings, number of unemerged parasitoids, number of unhatched spiderlings, and eggs with undeveloped embryos. Parasitoids and predators were identified to the genus or species level using published keys [25,45,46,47,48,49] and compared with specimens deposited in the Museo de Zoología, Universidad de Costa Rica (MZUCR). We deposited the voucher specimens of spiders and parasitoids at MZUCR. We took photographs of parasitoids with a Canon eos 80D and stacked images with HeliconFocus (HeliconSoft, Kharkiv, Ukraine) [50].

2.4. Data Analyses

To evaluate the effects of the urbanization level and the local environment (the immediate surroundings of the sampling sites) on the number of egg sacs parasitized and the proportion of parasitized eggs, we first created a model to compare these factors between the two species. This model included the number of parasitized egg sacs, the proportion of eggs parasitized as the response variable and urban category, PC1 (representing the immediate surroundings), season, building, and sampling date as random factors (Supplementary Material). In consecutive models, we evaluated the effects of urban category and immediate surroundings (PC1) on the number of egg sacs parasitized and the proportion of parasitized eggs for each species, with season, building, and sampling date included as random factors. In all cases, we used General Linear Mixed Models (GLMMs) with a Poisson error distribution for the number of egg sacs parasitized and a binomial error distribution for the proportion of eggs parasitized (R library Ime4) [51]. The two predictor factors, urban location, and the local environment were not collinear (the correlation between both factors varied between 0.18 and 0.46). Therefore, we maintained PC1 despite having a negligible effect since both factors were essential to test the predictions. In addition, we correlated the proportion of parasitized eggs and the number of emerging spiderlings using Spearman’s rank correlation. We performed all analyses using R statistical language (version 4.2.2, The R Foundation for Statistical Computing, Vienna, Austria) [52].

3. Results

3.1. Egg Sacs Parasitized

We collected 302 egg sacs from both spider species along the urban gradient during the study period: 161 from P. tepidariorum and 141 from L. geometricus (Figure 5). Parasteatoda tepidariorum parasitized more egg sacs, with a total of 62 egg sacs (38.5% of the egg sacs collected), than L. geometricus, with 17 egg sacs parasitized (12.1% of the egg sacs collected) (Table 1 section A).
We found P. tepidariorum in the three sampling sites and L. geometricus in two sampling sites: high and intermediate urbanization. For both species, the egg sacs were more parasitized in the site with intermediate urbanization, though for P. tepidariorum, this was only marginally significant (Figure 6; Table 1 section B). Neither species nor the surrounding environment (PC1) affected the number of parasitized egg sacs.

3.2. Proportion of Parasitism

The proportion of parasitized eggs was similar between P. tepidariorum and L. geometricus (Table 2 section A). In P. tepidariorum, this proportion did not differ along the urban gradient, but there was a larger proportion (marginally significant) of eggs parasitized during the rainy season (Table 2 section B). In contrast, L. geometricus had a higher, though not significant, proportion of parasitized eggs per sac in the intermediate-urban location; PC1 did not affect the proportion of parasitized eggs in either species (Table 2 ssection C).

3.3. Parasitoids

Two species of parasitoids in the family Scelionidae emerged from the egg sacs of P. tepidariorum: Baeus achaearaneus (Loiácono, 1973) and Idris sp. (Figure 7). These two wasps parasitized fifty-nine egg sacs: fifty-one by B. achaearaneus and eight by Idris sp.; both species emerged from the same sac on three occasions. Thus, B. achaearaneus was the most common parasitoid of P. tepidariorum, with a prevalence of 87% of all parasitized egg sacs. We did not find any egg predators in the egg sacs of this spider (Table 3).
For L. geometricus, we found two parasitoid wasps in the egg sacs: Philolema sp. (Eurytomidae) and Pediobius pyrgo (Walker, 1839) (Figure 7). The latter was the most common parasitoid, which emerged from eleven egg sacs (64.7%), while Philolema sp. emerged from five egg sacs. In one case, both parasitoids emerged from the same egg sac, and a predatory fly, Pseudogaurax sp. (Chloropidae), was found in one egg sac. Parasitoids correlated negatively with the number of spiders that emerged in P. tepidariorum (rs = −0.49, p < 0.001) and L. geometricus (rs = −0.50, p < 0.001); in both species, the number of spiderlings decreased as the proportion of eggs parasitized increased.

4. Discussion

Habitat affects the prevalence of parasitoids (egg sacs parasitized). Contrary to our expectations, we found the highest prevalence of parasitoids in the site with intermediate urbanization (Figure 5), and we did not find evidence that the prevalence of parasitoids is correlated with the degree of urbanization. Urbanization is responsible for modifying the interactions between groups of organisms [16,27], which may be essential for maintaining community stability [53,54,55,56].
There are at least two non-mutually exclusive possible explanations for the pattern observed. Urbanization could affect, positively or negatively, the food resources and the suite of environmental conditions for the dispersal, reproduction, and population maintenance of parasitoids [16]. It could also alter the equilibrium between natural enemies (e.g., microbes, predators, and parasitoids) and their hosts, thereby increasing or reducing their populations [57]. Therefore, urbanization may affect some species positively and others negatively, depending on the extent to which urbanization allows the survival of the parasitoids and hosts. The urban environment, dominated by buildings, roads, and other human-made structures, might function as a parasitoid dispersal barrier, limiting host finding [27]. The heat islands associated with urban environments could also reduce spiderling development and increase mortality [58]. The higher heat in urban environments may also affect the growth and mortality of some spider egg parasitoids less adapted to high temperatures [59]. Hence, the prevalent conditions in highly urbanized sites can affect spider parasitoids depending on their ecological requirements and tolerance [16,19].
Evidence shows that the elimination of natural habitats as urban development increases directly affects the composition, abundance, and function of arthropod natural enemies [55,60]. Thus, the success of parasitoids in accessing their hosts may also be affected by habitat connectivity and their tolerance to the urbanized environment (urban-tolerant species). Habitat specialist parasitoids require corridors to colonize patches with similar ecological conditions [27]. However, landscape heterogeneity favors urban-tolerant species because it permits generalist parasitoids to survive and move across larger areas while searching for hosts [9,55,61].
Although we know little about the ecological requirements of the parasitoids attacking the eggs of P. tepidariorum and L. geometricus, it is known that they tolerate a high degree of urbanization [19]. However, the parasitoids benefit from the conditions prevalent in sites with intermediate urbanization, suggesting that these parasitoids are urban-tolerant rather than specialists [60]. Indirect evidence from previous studies conducted in one of the study sites (UCR) supports this argument. In 1971, 48.5% of the egg sacs of P. tepidariorum were parasitized [23] when the area consisted of large tracts of secondary forest, early-growth vegetation, coffee plantations, and pastures, roughly similar to the less urbanized site in our study. In 2012, 65% of the egg sacs were parasitized [26] when the natural and seminatural vegetation area had been reduced to smaller tracts [6], like the intermediate site in the present study. In contrast, we found only 38.5% of the egg sacs parasitized in the same site, which is probably related to the recent conversion of most natural and seminatural areas into hardscapes.
Identifying the factors that explain the increasing prevalence of parasitism in locations with intermediate urban development has yet to be discovered. However, we can deduce that such factors are likely related to the resources (e.g., food) that intermediate urbanized habitat provides to adult parasitoids and their probability of accessing spider hosts in this habitat [16,27,61]. For P. tepidariorum, the lower number of egg sacs parasitized found in the low-urbanization site could be attributed to a reduced spider density, likely due to the scarcity of human-made structures (e.g., buildings and houses), which serve as the primary habitat of this spider in the study site, which is composed primarily of coffee and sugar cane plantations adjacent to forest patches (Figure 3). However, we cannot entirely discard the possibility that pesticides, used in some of the coffee farms in the area, harm spider parasitoid populations, as has been reported for other parasitoids [62,63,64,65,66].
We also found that the number of parasitoids in the egg sacs of L. geometricus was lower than in P. tepidariorum, which could be explained by several factors. L. geometricus is a relatively recent invader of the Americas [22,29,31], and species that spread into new regions experience a lower prevalence of parasites than native species [67]. In addition, L. geometricus constructs more protected egg-sac retreats than P. tepidariorum by laying sticky lines on the egg sac [20,34,39], which could limit the access of parasitoids to the eggs [26], and producing toxins in the egg sacs [68]. All these factors may protect the eggs of L. geometricus and reduce egg sac parasitism. Finally, the differences in the prevalence of parasitoids in egg sacs between the two spider species could also be due to differences in abundance, ecological requirements, or behavior of the parasitoids attacking the eggs of each spider species. However, further research is needed to test these possibilities.
The urban gradient did not affect the proportion of eggs parasitized within the egg sacs of P. tepidariorum and L. geometricus. We found a large variation in the proportion of parasitized eggs, which was similar in both spider species and across all sites (Table S2). This suggests that different factors drive the number of egg sacs parasitized versus the proportion of eggs parasitized within egg sacs. The prevalence of egg sacs parasitized is directly related to the probability of parasitoids finding egg sacs, which could be affected by at least three factors: abundance and density of egg sacs, age of the eggs (eggs can be parasitized for only a short period after being laid [69]), and abundance of parasitoids [70]. However, once a parasitoid finds an egg sac, the number of spider eggs attacked depends on other factors, like the number of eggs present in the parasitoid’s ovarioles, the number of female parasitoids that oviposit into a single egg sac, and the proportion of eggs within the sac that are accessible to the parasitoids.
In conclusion, since urbanization alters natural environments in various ways, we can begin to understand the differences in parasitoid prevalence in these spiders. The impact of anthropogenic changes on species interactions is likely related to the intensity (the percentage of the natural ecosystem replaced by hardscape), the extent (the area covered by urbanscape), and the time since the natural environment was modified. Low levels of urbanization may maintain species interaction dynamics (e.g., parasite-host equilibrium) similar to those in natural environments, and could even favor some generalist species tolerant of these conditions. Intermediate urbanization in this context favors parasitoids [27] by increasing their prevalence on spider eggs, and they may benefit from some of the changes due to urbanization if a significant fraction of the natural environment is still present. However, as urban development advances, the environment changes drastically (e.g., rising temperatures), and the connectivity between resource patches and access to spider eggs may be reduced [6,17]. Thus, environmental changes tied to urbanization and other anthropogenic alterations can affect not exclusively species diversity and abundance, but also the interactions between species.

Supplementary Materials

The following supporting information can be downloaded at the following website: https://www.mdpi.com/article/10.3390/arthropoda2040018/s1, Table S1: Percentage of agricultural patches, green areas, and human constructions in a buffer zone of 2.5 km surrounding each sampling site; Table S1: Mean number of female and male parasitoids per egg sac and their sex ratio.

Author Contributions

N.J.-C.: conceptualization, data collection, and analyses; writing the original draft. P.E.H.: review, data-visualization, editing, parasitoid wasp identification. E.C.-M.: review, data-visualization, and editing. G.R.-M.: review and help with data collection and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This research funding was provided by the Vice Rector´s Office for Research of the University of Costa Rica (UCR) in San José, Costa Rica to the research project number 111-C052 for the Gilbert Barrantes Lab project.

Data Availability Statement

The data analyzed in this research are available upon request from the corresponding author.

Acknowledgments

We thank Alejandro Vargas-Rodríguez for the identification of the predator fly that emerged in the L. geometricus egg sac and Andrés Arias-Paco (Museo de Insectos, CIPROC, Universidad de Costa Rica) for taking and editing the photographs of the parasitoid and Gilbert Barrantes for his support in data analysis and sampling design.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Durkin, E.S.; Cassidy, S.T.; Gilbert, R.; Richardson, E.A.; Roth, A.M.; Shablin, S.; Keiser, C.N. Parasites of spiders: Their impacts on host behavior and ecology. J. Arachnol. 2021, 49, 281–298. [Google Scholar] [CrossRef]
  2. Fei, M.; Gols, R.; Harvey, J.A. The bology and ecology of parasitoid wasps of predatory arthropods. Annu. Rev. Entomol. 2023, 68, 109–128. [Google Scholar] [CrossRef] [PubMed]
  3. Daniel, J.A.; Arabesky, V.; Rozenberg, T.; Lubin, Y.; Segoli, M.; Mowery, M.A. Parasitoid development and superparasitism in invasive versus native widow spider host egg sacs. Biol. Invasions 2023, 25, 2519–2530. [Google Scholar] [CrossRef]
  4. Austin, A.D. The function of spider egg sacs in relation to parasitoids and predators, with special reference to the Australian fauna. J. Nat. Hist. 1985, 19, 359–376. [Google Scholar] [CrossRef]
  5. Matsumoto, R.; Konishi, K. Life histories of two ichneumonid parasitoids of Cyclosa octotuberculata (Araneae): Reclinervellus tuberculatus (Uchida) and its new sympatric congener (Hymenoptera: Ichneumonidae: Pimplinae). Entomol. Sci. 2007, 10, 267–278. [Google Scholar] [CrossRef]
  6. Jervis, M.A.; Kidd, N.A.C. Host-feeding strategies in hymenopteran parasitoids. Biol. Rev. 1986, 61, 395–434. [Google Scholar] [CrossRef]
  7. Horváth, R.; Magura, T.; Tóthmérész, B. Ignoring ecological demands masks the real effect of urbanization: A case study of ground-dwelling spiders along a rural-urban gradient in a lowland forest in Hungary. Ecol. Res. 2012, 27, 1069–1077. [Google Scholar] [CrossRef]
  8. Argañaraz, C.I.; Gleiser, R.M. Does urbanization have positive or negative effects on Crab spider (Araneae: Thomisidae) diversity? Zoologia 2017, 34, e19987. [Google Scholar] [CrossRef]
  9. Shochat, E.; Lerman, S.B.; Anderies, J.M.; Warren, P.S.; Faeth, S.H.; Nilon, C.H. Invasion, competition, and biodiversity loss in urban ecosystems. BioScience 2010, 60, 199–208. [Google Scholar] [CrossRef]
  10. Alberti, M. Eco-evolutionary dynamics in an urbanizing planet. Trends Ecol. Evol. 2015, 30, 114–126. [Google Scholar] [CrossRef]
  11. Egerer, M.; Fairbairn, M. Gated gardens: Effects of urbanization on community formation and commons management in community gardens. Geoforum 2018, 96, 61–69. [Google Scholar] [CrossRef]
  12. Rodríguez-Bardía, M.; Fuchs, E.J.; Barrantes, G.; Madrigal-Brenes, R.; Sandoval, L. Genetic structure in neotropical birds with different tolerance to urbanization. Sci. Rep. 2022, 12, 6054. [Google Scholar] [CrossRef]
  13. Alberti, M. The effects of urban patterns on ecosystem function. Int. Reg. Sci. Rev. 2005, 28, 168–192. [Google Scholar] [CrossRef]
  14. Ramalho, C.E.; Hobbs, R.J. Time for a change: Dynamic urban ecology. Trends Ecol. Evol. 2012, 27, 179–188. [Google Scholar] [CrossRef] [PubMed]
  15. Becker, C.; Desneux, N.; Monticelli, L.; Fernandez, X.; Michel, T.; Lavoir, A.V. Effects of abiotic factors on HIPV-mediated interactions between plants and parasitoids. Biomed Res. Int. 2015, 2015, 342982. [Google Scholar] [CrossRef]
  16. Bennett, A.B.; Gratton, C. Local and landscape scale variables impact parasitoid assemblages across an urbanization gradient. Landsc. Urban Plan. 2012, 104, 26–33. [Google Scholar] [CrossRef]
  17. Finch, O.D. The parasitoid complex and parasitoid-induced mortality of spiders (Araneae) in a Central European woodland. J. Nat. Hist. 2005, 39, 2339–2354. [Google Scholar]
  18. Magura, T.; Horváth, R.; Tóthmérész, B. Effects of urbanization on ground-dwelling spiders in forest patches, in Hungary. Landsc. Ecol. 2010, 25, 621–629. [Google Scholar] [CrossRef]
  19. Moura, R.R.; Neto, A.T.; Gonzaga, M.O. Don’t put all your eggs in small baskets: Ineffective guardians, incidence of parasitoids and clutch size of Latrodectus geometricus (Araneae, Theridiidae) along an urban gradient. Zool. Anz. 2010, 295, 120–125. [Google Scholar] [CrossRef]
  20. Vetter, R.S.; Vincent, L.S.; Itnyre, A.A.; Clarke, D.E.; Reinker, K.I.; Danielsen, W.R.D.; Robinson, L.J.; Kabashima, J.M.; Rust, M.K. Predators and parasitoids of egg sacs of the widow spiders, Latrodectus geometricus and Latrodectus hesperus (Araneae: Theridiidae) in southern California. J. Arachnol. 2012, 40, 209–214. [Google Scholar] [CrossRef]
  21. Marie, J.; Vetter, R.S. Establishment of the brown widow spider (Araneae: Theridiidae) and infestation of its egg sacs by a parasitoid, Philolema latrodecti (Hymenoptera: Eurytomidae), in French Polynesia and the Cook Islands. J. Med. Entomol. 2015, 52, 1291–1298. [Google Scholar] [CrossRef] [PubMed]
  22. Vincent, L.S.; Vetter, R.S.; Wrenn, W.J.; Kempf, J.K.; Berrian, J.E. The brown widow spider Latrodectus geometricus CL Koch, 1841, in southern California. Pan-Pac. Entomol. 2009, 84, 344–349. [Google Scholar] [CrossRef]
  23. Valerio, C.E. Parasitismo en huevos de araña Achaearanea tepidariorum (Koch) (Aranea: Theridiidae) en Costa Rica. Rev. Biol. Trop. 1971, 18, 99–106. [Google Scholar]
  24. Valerio, C.E. Dimorfismo en avispas macho de la familia Scelionidae (Hymenoptera). Brenesia 1974, 1974, 1–9. [Google Scholar]
  25. Loiácono, M.S.; Margaría, C.B. Las especies del género Baeus (Hymenoptera: Scelionidae) endoparasitoides de ootecas de arañas en la región neotropical. Acta Zool. Mex. 2004, 20, 83–90. [Google Scholar] [CrossRef]
  26. Triana, E.; Barrantes, G.; Hanson, P.E. Incidence of parasitoids and predators on eggs of seven species of Theridiidae (Araneae). Arachnology 2012, 15, 293–298. [Google Scholar]
  27. Corcos, D.; Cerretti, P.; Caruso, V.; Mei, M.; Falco, M.; Marini, L. Impact of urbanization on predator and parasitoid insects at multiple spatial scales. PLoS ONE 2019, 14, e0214068. [Google Scholar] [CrossRef]
  28. Hanson, P.E.; Gauld, I.D. (Eds.) Hymenoptera de la Región Neotropical; Memoirs of the American Entomological Institute: Totnes, UK, 2006; Volume 77, pp. 1–997. [Google Scholar]
  29. Garb, J.E.; González, A.; Gillespie, R.G. The black widow spider genus Latrodectus (Araneae: Theridiidae): Phylogeny, biogeography, and invasion history. Mol. Phylogenetics Evol. 2004, 31, 1127–1142. [Google Scholar] [CrossRef]
  30. Taucare-Ríos, A. Primer registro de la viuda marrón, Latrodectus geometricus (Araneae: Theridiidae) en el norte de Chile. Rev. Chil. Entomol. 2011, 36, 39–42. [Google Scholar]
  31. Levi, H.W. Cosmopolitan and pantropical species of theridiid spiders (Araneae: Theridiidae). Pac. Insects 1967, 9, 175–186. [Google Scholar]
  32. Torchin, M.E.; Lafferty, K.D.; Dobson, A.P.; McKenzie, V.J.; Kuris, A.M. Introduced species and their missing parasites. Nature 2003, 421, 628–630. [Google Scholar] [CrossRef]
  33. Phillips, B.L.; Kelehear, C.; Pizzatto, L.; Brown, G.P.; Barton, D.; Shine, R. Parasites and pathogens lag behind their host during periods of host range advance. Ecology 2010, 91, 872–881. [Google Scholar] [CrossRef]
  34. Edwards, G.B. The Common House Spider, Parasteatoda tepidariorum (Koch) (Arachnida: Araneae: Theridiidae); University of Florida Institute of Food and Agricultural Sciences Extension: Gainesville, Florida, 2001; Volume 238, pp. 1–2. [Google Scholar]
  35. Mittmann, B.; Wolff, C. Embryonic development and staging of the cobweb spider Parasteatoda tepidariorum CL Koch, 1841 (syn.: Achaearanea tepidariorum; Araneomorphae; Theridiidae). Dev. Genes Evol. 2012, 222, 189–216. [Google Scholar] [CrossRef]
  36. McGregor, A.P.; Hilbrant, M.; Pechmann, M.; Schwager, E.E.; Prpic, N.M.; Damen, W.G. Cupiennius salei and Achaearanea tepidariorum: Spider models for investigating evolution and development. Bioessays 2008, 30, 487–498. [Google Scholar] [CrossRef]
  37. Taucare-Ríos, A.; Bizama, G.; Bustamante, R.O. Using global and regional species distribution models (SDM) to infer the invasive stage of Latrodectus geometricus (Araneae: Theridiidae) in the Americas. Environ. Entomol. 2016, 45, 1379–1385. [Google Scholar] [CrossRef]
  38. Barrantes, G.B. La viuda negra en Costa Rica: Información general. Biocenosis 2016, 30, 63–96. [Google Scholar]
  39. Vetter, R.S.; Penas, L.M.; Hoddle, M.S. Laboratory refugia preferences of the brown widow spider, Latrodectus geometricus (Araneae: Theridiidae). J. Arachnol. 2016, 44, 52–57. [Google Scholar] [CrossRef]
  40. Schoeninger, K.; de Pádua, D.G.; Salvatierra, L.; de Oliveira, M.L. First record of Pediobius pyrgo Walker (Hymenoptera: Eulophidae) in South America and its emergence from egg sacs of Latrodectus geometricus CL Koch (Araneae: Theridiidae). EntomoBrasilis 2015, 8, 79–81. [Google Scholar] [CrossRef]
  41. Taucare-Ríos, A.; Alvarenga, T.M.; Costa, V.A. Occurrence of Philolema sp. (Hymenoptera: Eurytomidae) in Latrodectus thoracicus (Nicolet, 1849) (Araneae: Theridiidae) egg sacs. Arachnology 2018, 17, 334–336. [Google Scholar] [CrossRef]
  42. QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation Project. 2019. Available online: https://qgis.org/ (accessed on 10 January 2024).
  43. Iqbal, M.; Austin, A. Systematics of the wasp genus Ceratobaeus Ashmead (Hymenoptera: Scelionidae) from Australasia: Parasitoids of spider eggs. Rec. South Aust. Mus. Monogr. Ser. 2000, 6, 1–164. [Google Scholar]
  44. Rasband, W.S. ImageJ; US National Institutes of Health: Bethesda, MA, USA, 1997–2016. Available online: https://imagej.nih.gov/ij/ (accessed on 10 January 2024).
  45. Masner, L. Revisionary notes and keys to world genera of Scelionidae (Hymenoptera: Proctorupoidea). Mem. Entomol. Soc. Can. 1976, 108, 1–87. [Google Scholar] [CrossRef]
  46. Hansson, C. Eulophidae of Costa Rica, 1; Memoirs of the American Entomological Institute: Logan, UT, USA, 2002; Volume 67, pp. 1–292. [Google Scholar]
  47. Gibson, G.A.P.; Huber, J.T.; Woolley, J.B. Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera); National Research Council Research Press: Ottawa, ON, Canada, 1997; pp. 1–794. [Google Scholar]
  48. Lotfalizadeh, H.; Delvare, G.; Rasplus, J.Y. Phylogenetic analysis of Eurytominae (Chalcidoidea: Eurytomidae) based on morphological characters. Zool. J. Linn. Soc. 2007, 151, 441–510. [Google Scholar] [CrossRef]
  49. Wheeler, T.A. Chloropidae. In Manual of Central American Diptera, 1st ed.; Brown, B.V., Borkent, A., Cumming, J.M., Wood, D.M., Woodley, N.E., Zumbado, M.A., Eds.; National Research Council: Ottawa, ON, Canada, 2010; Volume 2, pp. 1137–1153. [Google Scholar]
  50. Helicon Focus (RRID: SCR_014462) Editing Photographs Program. Available online: https://www.heliconsoft.com/focus/help/spanish/HeliconFocus.html (accessed on 21 October 2024).
  51. Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Soft. 2015, 67, 1–48. [Google Scholar] [CrossRef]
  52. R Development Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2020; Available online: www.R-project.org (accessed on 10 January 2024).
  53. Odum, E.P. Fundamentals of Ecology; W. B. Saunders Co.: Philadelphia, PA, USA, 1953; pp. 1–384. [Google Scholar]
  54. Elton, C.S. Ecology of Invasions by Animals and Plants; Chapman and Hall: London, UK, 1958; pp. 7–261. [Google Scholar]
  55. Clavel, J.; Julliard, R.; Devictor, V. Worldwide decline of specialist species: Toward a global functional homogenization? Front. Ecol. Environ. 2011, 9, 222–228. [Google Scholar] [CrossRef]
  56. Landi, P.; Minoarivelo, H.O.; Brännström, Å.; Hui, C.; Dieckmann, U. Complexity and stability of ecological networks: A review of the theory. Popul. Ecol. 2018, 60, 319–345. [Google Scholar] [CrossRef]
  57. Landis, D.A.; Wratten, S.D.; Gurr, G.M. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 2000, 45, 175–201. [Google Scholar] [CrossRef]
  58. Johnson, J.C.; Urcuyo, J.; Moen, C.; Stevens, D.R. Urban heat island conditions experienced by the Western black widow spider (Latrodectus hesperus): Extreme heat slows development but results in behavioral accommodations. PLoS ONE 2019, 14, e0220153.m. [Google Scholar] [CrossRef]
  59. Damien, D.; Pierre, J.S.; van Baaren, J.; van Alphen, J.J.M. How temperature and habitat quality affect parasitoid lifetime reproductive success—A simulation study. Ecol. Modell. 2011, 222, 1604–1613. [Google Scholar]
  60. Burkman, C.E.; Gardiner, M.M. Urban greenspace composition and landscape context influence natural enemy community composition and function. Biol. Control 2014, 75, 58–67. [Google Scholar] [CrossRef]
  61. Rudd, H.; Vala, J.; Schaefer, V. Importance of backyard habitat in a comprehensive biodiversity conservation strategy: A connectivity analysis of urban green spaces. Restor. Ecol. 2002, 10, 368–375. [Google Scholar] [CrossRef]
  62. Rojas, M. Manejo sostenible de la broca del café (Hypothenemus hampei) mediante poda sistemática del cafeto en Costa Rica. Agron. Costarric. 2012, 36, 71–79. [Google Scholar] [CrossRef]
  63. Monge, P.; Partanen, T.; Wesseling, C.; Bravo, V.; Ruepert, C.; Burstyn, I. Assessment of pesticide exposure in the agricultural population of Costa Rica. Ann. Occup. Hyg. 2005, 49, 375–384. [Google Scholar] [PubMed]
  64. Blackman, A.; Naranjo, M.A. Does eco-certification have environmental benefits? Organic coffee in Costa Rica. Ecol. Econ. 2012, 83, 58–66. [Google Scholar] [CrossRef]
  65. Guido Cruz, F.; Castro Sánchez, S. Viviendo con la crisis cafetalera: Perspectivas futuras de pequeños y medianos productores de café en San Ramón de Alajuela, Costa Rica. InterSedes 2011, 7, 11–28. [Google Scholar]
  66. Pinheiro, L.A.; Dader, B.; Wanumen, A.C.; Pereira, J.A.; Santos, S.A.P.; Medina, P. Side Effects of pesticides on the Olive Fruit Fly parasitoid Psyttalia concolor (Szepligeti): A Review. Agronomy 2020, 10, 1755. [Google Scholar] [CrossRef]
  67. Mowery, M.A.; Arabesky, V.; Lubin, Y.; Segoli, M. Differential parasitism of native and invasive widow spider egg sacs. Behav. Ecol. 2022, 33, 565–572. [Google Scholar] [CrossRef]
  68. Schmidt, J.O.; Vetter, R.S.; Howe, A.K. Egg toxicity in diverse spider taxa. J. Arachnol. 2017, 45, 209–212. [Google Scholar] [CrossRef]
  69. Austin, A.D. The fecundity, development and host relationships of Ceratobaeus spp. (Hymenoptera: Scelionidae), parasites of spider eggs. Ecol. Entomol. 1984, 9, 125–138. [Google Scholar] [CrossRef]
  70. Barrantes, G.; Eberhard, W.G.; Weng, J.L. Seasonal patterns of parasitism of the tropical spiders Theridion evexum (Araneae, Theridiidae) and Allocyclosa bifurca (Araneae, Araneidae) by the wasps Zatypota petronae and Polysphincta gutfreundi (Hymenoptera, Ichneumonidae). Rev. Biol. Trop. 2008, 56, 749–754. [Google Scholar] [CrossRef] [PubMed]
Arthropoda 02 00018 g001
Figure 1. Spider species. (A) Parasteatoda tepidariorum with an egg sac. (B) Latrodectus geometricus wrapping a prey (Kenji Nishida, 19 December 2007).
Figure 1. Spider species. (A) Parasteatoda tepidariorum with an egg sac. (B) Latrodectus geometricus wrapping a prey (Kenji Nishida, 19 December 2007).
Arthropoda 02 00018 g001
Arthropoda 02 00018 g002
Figure 2. Map of the three sampling sites, indicated by red spots. All sites are in the western section of the Costa Rican Central Valley.
Figure 2. Map of the three sampling sites, indicated by red spots. All sites are in the western section of the Costa Rican Central Valley.
Arthropoda 02 00018 g002
Arthropoda 02 00018 g003
Figure 3. Different types of cover with a buffer zone of 2.5 km around the three sampling sites are indicated by red spots. (A) Low urbanization: Concepcion, San Ramon, a village with abundant agricultural areas and forest patches. (B) Intermediate urbanization: Occidental Campus of the University of Costa Rica, with a similar proportion of green cover, agricultural patches, and human constructions. (C) High urbanization: The Central Campus of the University of Costa Rica has the least green cover. We used Google Earth images from 2018 and QGIS to classify the cover shapes.
Figure 3. Different types of cover with a buffer zone of 2.5 km around the three sampling sites are indicated by red spots. (A) Low urbanization: Concepcion, San Ramon, a village with abundant agricultural areas and forest patches. (B) Intermediate urbanization: Occidental Campus of the University of Costa Rica, with a similar proportion of green cover, agricultural patches, and human constructions. (C) High urbanization: The Central Campus of the University of Costa Rica has the least green cover. We used Google Earth images from 2018 and QGIS to classify the cover shapes.
Arthropoda 02 00018 g003
Arthropoda 02 00018 g004
Figure 4. Diagram of the method used to determine the local scale variables. A panoramic photograph of the section of the building was taken, and the type of cover for each photograph (taken at 10 m from the building) were quantified.
Figure 4. Diagram of the method used to determine the local scale variables. A panoramic photograph of the section of the building was taken, and the type of cover for each photograph (taken at 10 m from the building) were quantified.
Arthropoda 02 00018 g004
Arthropoda 02 00018 g005
Figure 5. The number of parasitized and unparasitized egg sacs for Latrodectus geometricus and Parasteatoda tepidariorum.
Figure 5. The number of parasitized and unparasitized egg sacs for Latrodectus geometricus and Parasteatoda tepidariorum.
Arthropoda 02 00018 g005
Arthropoda 02 00018 g006
Figure 6. The number of parasitized and unparasitized egg sacs for each spider species along an urban gradient of high, intermediate, and low urbanization. (A) Parasteatoda tepidariorum and (B) Latrodectus geometricus.
Figure 6. The number of parasitized and unparasitized egg sacs for each spider species along an urban gradient of high, intermediate, and low urbanization. (A) Parasteatoda tepidariorum and (B) Latrodectus geometricus.
Arthropoda 02 00018 g006
Arthropoda 02 00018 g007
Figure 7. Parasitoid species. (A) Baeus achaearaneus ♀ and (B) Idris sp. ♀ (both Scelionidae) emerged from Parasteatoda tepidariorum egg sacs. (C) Pediobius pyrgo ♂ (Eulophidae) and (D) Philolema sp. ♀ (Eurytomidae) emerged from Latrodectus geometricus egg sacs.
Figure 7. Parasitoid species. (A) Baeus achaearaneus ♀ and (B) Idris sp. ♀ (both Scelionidae) emerged from Parasteatoda tepidariorum egg sacs. (C) Pediobius pyrgo ♂ (Eulophidae) and (D) Philolema sp. ♀ (Eurytomidae) emerged from Latrodectus geometricus egg sacs.
Arthropoda 02 00018 g007
Table 1. Comparison of egg sacs parasitized between the spider species and along an urban gradient for each spider species (Parasteatoda tepidariorum and Latrodectus geometricus), based on GLMM. The lower (LCI) and upper (UCI) 95% confidence intervals are included. Boldface indicates coefficients that are significantly different from zero and uppercase letters delimit sections for each species and between species comparisons.
Table 1. Comparison of egg sacs parasitized between the spider species and along an urban gradient for each spider species (Parasteatoda tepidariorum and Latrodectus geometricus), based on GLMM. The lower (LCI) and upper (UCI) 95% confidence intervals are included. Boldface indicates coefficients that are significantly different from zero and uppercase letters delimit sections for each species and between species comparisons.
EffectCoefficientsSELCIUCI
A Between species
Intercept−1.070.29−1.63−0.51
L. geometricus−1.230.34−1.90−0.55
B Parasteatoda tepidariorum
Intercept−1.070.310.461.68
Inter. Urbanization0.540.30−0.061.14
Low urbanization−0.660.91−2.441.11
PC10.090.22−0.340.52
C Latrodectus geometricus
Intercept−2.800.45−3.68−1.92
Inter. Urbanization1.200.550.132.28
PC10.070.15−0.220.36
Table 2. Comparison of parasitized egg proportions in Parasteatoda tepidariorum and Latrodectus geometricus and along an urban gradient for each spider species, based on GLMM. The lower (LCI) and upper (UCI) 95% confidence intervals are included. Uppercase letters delimit sections for each species and between species comparisons.
Table 2. Comparison of parasitized egg proportions in Parasteatoda tepidariorum and Latrodectus geometricus and along an urban gradient for each spider species, based on GLMM. The lower (LCI) and upper (UCI) 95% confidence intervals are included. Uppercase letters delimit sections for each species and between species comparisons.
EffectCoefficientsSELCIUCI
A Between species
Intercept−2.150.55−3.22−1.08
L. geometricus−0.920.81−2.500.66
B Parasteatoda tepidariorum
Intercept−1.420.46−2.31−0.52
Inter. Urbanization0.220.49−0.741.18
Low urbanization−1.921.46−4.790.95
PC10.120.32−0.510.75
C Latrodectus geometricus
Intercept−5.251.91−9.00−1.50
Inter. Urbanization2.811.85−0.816.44
PC10.000.22−0.440.44
Table 3. Total egg sacs collected from Parasteatoda tepidariorum and Latrodectus geometricus, parasitoid species, and the percentage of parasitized egg sacs. The identity of parasitoids and egg predators are included.
Table 3. Total egg sacs collected from Parasteatoda tepidariorum and Latrodectus geometricus, parasitoid species, and the percentage of parasitized egg sacs. The identity of parasitoids and egg predators are included.
UrbanismNumber of Egg Sacs Parasitized Total Egg SacsPercentage of Egg Sacs ParasitizedParasitoids Predators
(A) Parasteatoda tepidariorum
High 216731.3Baeus achaeraneus
Idris sp.		No
Intermediate335856.9
Low 83622.2
(B) Latrodectus geometricus
High 5845.9Philolema sp. Pediobius pyrgo Pseudogaurax sp.
Intermediate125721.0
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Jiménez-Conejo, N.; Hanson, P.E.; Chacón-Madrigal, E.; Rojas-Malavasi, G. The Prevalence of Egg Parasitoids of Two Cobweb Spiders in a Tropical Urban Gradient. Arthropoda 2024, 2, 250-263. https://doi.org/10.3390/arthropoda2040018

AMA Style

Jiménez-Conejo N, Hanson PE, Chacón-Madrigal E, Rojas-Malavasi G. The Prevalence of Egg Parasitoids of Two Cobweb Spiders in a Tropical Urban Gradient. Arthropoda. 2024; 2(4):250-263. https://doi.org/10.3390/arthropoda2040018

Chicago/Turabian Style

Jiménez-Conejo, Natalia, Paul E. Hanson, Eduardo Chacón-Madrigal, and Geovanna Rojas-Malavasi. 2024. "The Prevalence of Egg Parasitoids of Two Cobweb Spiders in a Tropical Urban Gradient" Arthropoda 2, no. 4: 250-263. https://doi.org/10.3390/arthropoda2040018

APA Style

Jiménez-Conejo, N., Hanson, P. E., Chacón-Madrigal, E., & Rojas-Malavasi, G. (2024). The Prevalence of Egg Parasitoids of Two Cobweb Spiders in a Tropical Urban Gradient. Arthropoda, 2(4), 250-263. https://doi.org/10.3390/arthropoda2040018

Article Metrics

Back to TopTop