Abstract
Ladybirds (Coleoptera: Coccinellidae) are a significant predator group that plays a role in agricultural contexts. They serve as important biocontrol agents against several agricultural pests. However, there is limited information available about how ladybirds’ populations are regulated by their natural enemies and habitat perturbation. In this study, we evaluated ladybird communities associated with natural and managed areas during the agricultural cycle of 2018 (June–September). We identified seven ladybird species; the most abundant species were Hippodamia convergens (70% individuals) and Cycloneda sanguinea (20% individuals), followed by the exotic species Harmonia axyridis (3.33% individuals), while Paranaemia vittigera, Coleomegilla maculata, Brachiacantha sp., and Olla v-nigrum represented less than 3% each. Ladybirds were more abundant in agricultural fields than in natural habitats. We identified several natural enemies associated with the collected ladybirds, including parasitoids (Dinocampus coccinellae, Hymenoptera: Braconidae), ectoparasitic Acari (Coccipolipus sp., Podapolipidae), and nematodes (Mermithidae). However, none of the natural enemies affected more than 10% of the ladybirds, so natural enemies do not appear to be exerting substantial control over their populations. Our results corroborated that ladybirds can efficiently thrive in anthropogenic habitats in Mexico and therefore may represent good biocontrol agents for agriculture. It is important to consider the ecology of agriculturally important ladybirds in programs for integrated pest management. This includes factors contributing to the mortality of ladybirds, including their natural enemies.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Ladybirds are important predators of a wide range of insect herbivores of economic relevance, such as aphids, whiteflies, scales, bugs, moth larvae, and some mites (Honěk et al. 2017). Depending on food availability and the season, some ladybird species are also able to feed on pollen, nectar, fungal spores, plant tissue, or resort to cannibalism if necessary (Escalona et al. 2017). As such, predaceous ladybirds have been widely used as pest regulators in agricultural systems (Obrycki et al. 2009).
The use of biocontrol agents represents an economical and environmentally friendlier alternative to the increasing use of chemical insecticides to control pests (van Lenteren et al. 2018). It has been estimated that the total economic value of the control of economically important insect pests provided by natural enemies in the USA is $4.5 billion per year (Losey and Vaughan 2006), and the economic value of the ecosystem service provided by predaceous ladybirds in soybean cultures is $239 million (Landis et al. 2008; Ameixa et al. 2018; Soares et al. 2023). In Mexico, predaceous ladybirds are considered to be important biocontrol agents (Rodríguez et al. 2015), but there are no economic estimates available. Ladybirds provide critical ecosystem services, especially herbivore regulation, which is crucial in agroecosystems. Ladybirds can eat up to hundred aphids per day and substantially reduce crop losses, depending on the species (Shrestha and Parajulee 2013; Ramzan and Khursheed 2023). Ladybirds are known to significantly reduce populations of mites (Acari: Tetranychidae); and the members of the hemipteran suborder Sternorrhyncha, including aphids, adelgids, scales, mealybugs, whiteflies, and psyllids (Biddinger et al. 2009; Giorgi et al. 2009; Hodek and Honěk 2009). The ecosystem service provided by predaceous ladybirds is influenced by factors such as land-use change, agricultural intensification and the associated increase in chemical pesticide application (Bianchi et al. 2006; Honěk et al. 2017), climate change (Sloggett 2021), urbanization (Grez et al. 2019), light pollution (Miller et al. 2017), invasive species (Brown and Roy 2018), as well as regulation by their natural enemies (Iperti 1999).
Natural enemies of ladybirds
The main agents that control ladybird populations are parasitoids, parasites, and pathogens (Ceryngier et al. 2012, 2018; Riddick et al. 2009; Haelewaters et al. 2017). Known ladybird parasitoids include species of Hymenoptera (Braconidae, Encyrtidae, Pteromalidae, Eulophidae, among others) and Diptera (Phoridae, Tachinidae, Sarcophagidae among others (Ceryngier et al. 2012; Riddick et al. 2009)). The most cited ladybird parasitoid is Dinocampus coccinellae (Braconidae: Euphorinae), which is a solitary wasp and generalist endoparasitoid with a cosmopolitan distribution (Ceryngier et at. 2023). This species has been widely studied and is known to attack at least 72 ladybird species. The most frequently attacked hosts worldwide are Coccinella septempunctata, Harmonia axyridis, Coleomegilla maculata, and Hippodamia convergens (Ceryngier et al. 2023; Bjørnson 2008; Riddick et al. 2009; Silva et al. 2012; Wharton et al. 1997). Dinocampus coccinellae most frequently reproduces by thelytoky, by which diploid females develop from unfertilized eggs (Sethuraman et al. 2022). Dinocampus coccinellae presents a symbiotic relationship with a specific RNA virus called the Dinocampus coccinellae paralysis virus, which is transmitted from the parasitoid larva to the ladybird cerebral ganglia and paralyzes the host once the larvae are ready to pupate on the outside of the host. Once in the outside, the larvae pupate between the legs of the ladybird where it is protected against predators and hyperparasitoids until it emerges (Fei et al. 2023; Dheilly et al. 2015).
In the case of parasites, ladybirds are known to be parasitized by ectoparasitic mites, nematodes, entomopathogenic fungi, bacteria, and viruses (Ceryngier et al. 2012; Roy et al. 2011). Podapolipidae (Acari) can attack various groups of hosts. Highly specialized parasites of Coccinellidae are those of the genus Coccipolipus. (Ceryngier et al. 2012; McDaniel and Morrill 1969; Ramaraju and Poorani 2012; Riddick 2010; Rhule et al. 2010). Coccipolipus hippodamiae has been found parasitizing Adalia bipunctata, Hi. convergens, Ha. axyridis, and Cy. sanguinea among others (Ceryngier et al. 2012; Rhule et al. 2010). Adult females of this ectoparasitic mite are non-motile and remain attached to the ladybird´s elytra feeding upon host hemolymph throughout its development. When the mites reach maturity, they lay their eggs which give rise to motile larvae that migrate to a new host during ladybird copulation (Ceryngier et al. 2012). Infestation with these mites has negative effects including decreased hatching success of ladybird eggs, reduced female fertility, and decreased male survivorship during overwintering (Shaikevich et al. 2023; Webberley et al. 2004). Ectoparasitic C. hippodamie mites can also be vector of endosymbiotic bacteria Spiroplasma and Wolbachia that can infect ladybirds (Li et al. 2021; Shaikevich et al. 2023).
Ladybirds are also known to be parasitized by Laboulbeniales fungi, which are microscopic obligated arthropod ectoparasites that never form mycelium (Haelewaters et al. 2021). Ladybirds are infected by several species of the genus Hesperomyces. For example, Hesperomyces virescens is known to infect up to 30 host species, but in reality, constitutes a complex of multiple species segregated by host and geography. Hosts include Cy. sanguinea, Ha. axyridis, Hi. convergens, and Olla v-nigrum (Haelewaters et al. 2018, 2022; Van Caenegem et al. 2023). Thus far, the following species are described in this complex: He. halyziae, He. harmoniae, and He. parexochomi (Crous et al. 2021; Haelewaters and De Kesel 2020; Haelewaters et al. 2022). Hesperomyces spp. have a negative effect on ladybird survival under laboratory conditions (Haelewaters et al. 2020), as well as different negative effects when the host is affected by several natural enemies (Awad et al. 2023; de Groot and Haelewaters 2022). Other fungi of the Order Hypocreales, particularly Beauveria bassiana, have been widely studied because they cause high mortality in overwintering ladybirds (Ceryngier et al. 2012; Roy et al. 2011). Additionally, Metarhizium anisopliae, Cordyceps farinosa, Cordyceps fumosorosea, and Akanthomyces lecanii are known to interact with ladybirds. The infection caused by these entomopathogenic fungi starts with conidia adhesion, germination, and penetration to the host cuticle. Their life-cycle is hemibiotrophic–biotrophic as parasites in the host hemocoel, and saprophytic once the host is dead (Ceryngier et al. 2012). Some ladybirds known to be parasitized by these fungi are A. bipunctata, Coc. septempunctata, Ha. axyridis, and O. v-nigrum (Roy et al. 2008).
Several nematode families parasitize ladybirds, mainly Allantonematidae and Mermithidae (Ceryngier et al. 2012, 2018). Mermithids are known to parasitize of 15 orders of insects (Nickle 1972) including Hemiptera (Cicadellidae, Pentatomidae, Aphididae; Rusconi et al. 2020; Watanabe et al. 2021), Lepidoptera (Noctuidae; Sun et al. 2020), Diptera (Lourdes et al. 2023), and Coleoptera. The Mermithidae that parasitize ladybirds are solitary endoparasitic nematodes that attack adult insect hosts and emerge as last instar larvae (Ceryngier et al. 2012). This parasitism impacts host weight, respiratory frequency, and fat body and can cause physical damage to ladybird´s vital organs. Additionally, female hosts reduce their food intake, and sometimes becoming hyperactive. Once the nematodes complete their larval development inside the host, the ladybird is paralyzed and subsequently killed, and the nematode emerges (Ceryngier et al. 2012).
Ladybirds and the landscape
Natural landscapes have been transformed into anthropogenic, significantly simplified landscapes, affecting biodiversity (Morteo-Montiel et al. 2021). Agricultural intensification, deforestation, fragmentation, and land-use changes have also impacted ecosystem services, including the natural biocontrol of economically relevant herbivorous insects (Bianchi et al. 2006). Even though ladybirds have been recognized as important biocontrollers in Mexico (Rodríguez et al. 2015), there is limited information available about their natural population status and the potential threats to their communities related to habitat transformation in the country. Therefore, in this study, we aimed to evaluate ladybird communities in a transformed landscape that included both natural and anthropogenic habitats. Specifically, our goal was to understand whether ladybird abundance and parasitism rates were related to habitat transformation.
Materials and methods
Study site
Our study was performed within the Cuitzeo Lake Basin, which is located in the states of Michoacán and Guanajuato, Mexico. The basin encompasses an area of 3 847.61 km2, with an altitude range between 1830 and 3428 m a.s.l. The weather is warm with rains during summer. Temperature ranges between 17 and 25 °C, and mean annual precipitation is 778.4 mm (INEGI 2020). Most of the basin’s surface is covered with urban areas, agricultural fields, and fallow lands, but there are some remnants of native forest and matorral shrubland (Correa et al. 2014). We arbitrarily selected five areas distributed in the basin that each had three habitat types: (1) Agriculture with rainfed maize, (2) Fallow agricultural lands covered with herbaceous vegetation, and (3) Matorral with shrubs and small deciduous trees. In each zone, we selected a 1 ha plot per habitat type (N = 15 plots).
Ladybird sampling
Adult ladybirds were collected from the field by hand during the agricultural cycle between June and September 2018. The sampling was carried out in each habitat type per zone once each month (n = 15 plots/month). We divided 1-ha plots into four 0.25-ha sections, which were each surveyed by one person during each sampling event. Each person followed linear transects actively looking for coccinellids on the vegetation, stop** after 2.5 h or after finding 20 individuals of each ladybird species detected. We stopped at 20 individuals because we did not want to impact coccinellid populations in the field, considering the general decline in insect communities. Sampling was done between 8:00 and 13:00 h. Collected individuals were divided into two sets: the first 15 individuals collected of a given species were disinfected with sodium hypochlorite solution at 0.05%, held individually in perforated 30 ml plastic cups, and brought back to the laboratory to examine for parasitoids and endoparasitoids (the disinfection was intended to allow the characterization of entomopathogenic fungi; however, these data are not presented here). Any additional individuals were preserved in 70% ethanol to look for ectoparasites under the microscope.
Parasitoids and fungal infection
To evaluate parasitism rates, all individualized ladybirds in the lab were monitored and fed daily with wild aphids (Melanaphis sacchari, Myzus persicae, or Rhopalosiphum padi) until their death or until a period of 40 days had elapsed. They were kept under conditions of room temperature and ambient light (24 ± 2 °C and 12 h day/12 h night). For each host species, the results were evaluated in terms of percentages of successfully parasitized lady beetles. Once the parasitoid larvae emerged from the ladybird, we followed its fate daily until it reached adulthood, then they were preserved in 100% ethanol for its subsequent identification. The parasitoids were identified using Wharton et al. (1997). In these ladybirds, we also screened for the presence of thalli of Hesperomyces.
Nematodes
Nematodes that emerged from the ladybird hosts in the laboratory were preserved in 70% ethanol. Nematode molecular identification using barcoding was performed at the Colección Nacional de Helmintos, Instituto de Biología-UNAM.
Ectoparasites
We estimated ectoparasite occurrence by examining the ladybird specimens preserved in ethanol. We removed the elytra of all individuals, separating by species and plot, and examined them under 40 × magnification in a stereoscopic microscope (Carl Zeiss). Mites found under the elytra were preserved in 70% ethanol. Sampled mites were clarified with lactophenol at room temperature for 5 min. Then, the specimens were treated with Hoyer medium, covered with a circular plate, and left in an oven for 2–3 days at 40-50 °C until the sample medium had dried. Finally, the specimens were sealed with nail polish (Krantz and Walter 2009). The prepared specimens were observed under a phase contrast microscope and identified based on the key for mite families by Krantz and Walter (2009) and the key to Podapolipidae by Husband (1972). Taxonomic identification was performed at the Colección Nacional de Ácaros, Instituto de Biología-UNAM.
Statistical analysis
Ladybird abundance was analyzed with a nested ANOVA using habitat type, month, and their interaction as explanatory variables and zone and sampling period as nesting factors. The number of parasitized ladybirds was also analyzed with a nested ANOVA considering ladybird species, habitat type, and month as explanatory variables. Total abundances and number of parasitized ladybirds were log-transformed prior to analysis to comply with ANOVA assumptions (normality of errors and variance homoscedasticity). We checked for these assumptions by plotting the residuals against the fitted values (homoscedasticity) and plotting the errors against the theoretical quantiles (Q–Q plot) for each nesting level, as recommended by Crawley (2012). Parasitism by D. coccinellae was also compared among ladybird species and habitat types using a glm with poisson error. All analyses were performed using R with the glm package (R Core Team 2019).
Results
During our sampling period, we found a total of 596 ladybird individuals belonging to seven species in the three sampled habitats. The most abundant species was Hi. convergens (70% of individuals), followed by Cy. sanguinea (20%), the exotic Ha. axyridis (3.35%), and P. vittigera (3%), Brachiacantha sp. (2.5%), Col. maculata, and O. v-nigrum (less than 1% each) (Table 1).
There were temporal differences in ladybird abundance throughout our sampling period (F(3,36) = 4.618, p = 0.0152). July and August had the highest number of individuals in all habitats (208 and 198 ladybirds, respectively), while September had the lowest (79 individuals; Table 1).
Habitat type significantly affected ladybird abundance and community composition (F(2,12) = 9.81, p = 0.014); the highest number of ladybird individuals was found in agricultural and fallow lands (93%), while the matorral had low ladybird abundance. Ladybird richness was similar among habitats (five species in each), but species composition changed, Col. maculata and P. vittigera were only present in agricultural plots, while Ha. axyridis was only observed in fallow land plots.
Natural enemies
We found three types of natural enemies attacking the sampled ladybirds (Fig. 3), we did not find the presence of Hesperomyces in any of the sampled ladybirds. The parasitoid Dinocampus coccinellae (Schrank 1802) (Hymenoptera: Braconidae: Euphorinae) was the most prevalent (8%, 38 individuals parasitized out of 472), followed by a nematode of the Mermithidae family (10 individuals) and Coccipolipus spp. mites (Acari: Trombidiformes: Podapolipidae), present in 8 of the 19 analyzed samples (Table 2). Hippodamia convergens was affected by all the natural enemies, P. vittigera by nematodes and mites, and Cy. sanguinea and Col. maculata by the parasitoid, while Ha. axyridis, O. v-nigrum, and Brachiacantha sp. were not attacked by any natural enemy (Fig. 1).
a Ladybird natural enemies from the Cuitzeo Basin, Michoacán, Mexico. Three types of natural enemies were found: parasitoid D. coccinellae; nematode of the Mermithidae family; and Coccipolipus mites. b Abundance of each natural enemy (upper) and percent ladybird abundance per species (lower)
Dinocampus coccinellae showed different rates of emergence among the ladybird species (X2 = 29.2, df = 2, p < 0.001); 35 individuals of Hi. convergens (10%), two of Cy. sanguinea (1.7%) and one Col. maculata (20%). This parasitoid also differed in emergence among habitats (X2 = 58.69, df = 2, p < 0.001), with higher abundance in the agricultural and fallow habitats (Fig. 2).
Number of individuals parasitized by D. coccinellae per habitat type per species. Total abundance per species per habitat is shown in brackets
Mermithidae nematodes parasitized only two out of seven ladybird species and only 2.08% of the total ladybird individuals observed for this interaction (11/528). These were mostly in Hi. convergens (10 individuals), plus one P. vittigera individual, and nematodes were only detected in ladybirds from agricultural and fallow habitats. This study represents the first report of this family of nematodes attacking ladybirds in Mexico (Fig. 3).
Natural enemies of predatory ladybirds from the Cuitzeo basin, Michoacán, Mexico. a Adult Hi. convergens entrapped by the pupa of the parasitoid D. coccinellae, b Adult Hi. convergens containing by the larva of a nematode of the family Mermithidae, c Adult Hi. convergens with mites of the genus Coccipolipus. All photographs were taken by the authors, under a Carl Zeiss stereoscopic microscope
Ectoparasitic mites of the genus Coccipolipus were present in 8 of the 19 analyzed ladybird samples. Again, most of them were found on Hi. convergens (7), plus one on P. vittigera, and only from agricultural and fallow habitats.
Discussion
Our study showed that ladybirds were particularly abundant and diverse in agricultural and fallow fields. Almdal and Costamagna (2023) have also found that ladybird abundance is higher in crops due to higher aphid population sizes; we did not quantify aphid population size at our sites, but we did observe higher apparent aphid and scale insect abundance (Pers. Obs.). We therefore concur that annual crops likely have high food availability for ladybirds. This finding is important, since other studies have found that diverse ladybird communities are linked to more effective control of pest herbivores than communities with few species (Grez et al. 2021). Meanwhile, natural habitats such as matorrals had low ladybird abundance during the crop growing season when we sampled, but may serve as refuges for ladybirds during winter, as has been found in Europe (Holecová et al. 2018) or Canada (Labrie et al. 2008). This hypothesis warrants further investigation, beginning with sampling during the non-growing season at our study sites.
In our study site, we found seven species out the 21 reported to date for the state of Michoacán (López-Piña and Ponce-Saavedra 2017) and 213 reported for Mexico. Hippodamia convergens and Cy. sanguinea were the most abundant and common species, particularly in agricultural and fallow habitats. This is similar to results from Fortoul-Díaz et al. (2020) and Rodríguez-Del-Bosque et al. (2018), which were performed in sorghum agricultural fields. The exotic Ha. axyridis was only present in fallow habitats. We have observed its affinity for disturbed areas in Mexico (del-Val pers. obs.) as other studies in Latin-America have shown (Grez et al. 2013). It is worth noting that Ha. axyridis was introduced throughout the world as biocontrol for pests in crop fields, which is now the subject of strong controversy since it has displaced native ladybirds in many countries and its efficiency as a biocontrol agent is not particularly high (Camacho-Cervantes et al. 2021, 2017; Gardiner et al. 2009). We were expecting to find high abundances of Ha. axyridis in several sites since in previous years they were reported in different places, but it was not the case. Weather conditions or land-use changes in the area were not significantly different from previous years so there is a need of further investigation in those aspects. Regarding ladybird abundance recorded in matorrals, it should be considered as a minimum estimate, since we only sampled individuals associated with vegetation up to 2 m, and clearly more species or individuals may be found at other shrub/tree heights.
Natural enemies of ladybirds
Ladybird natural enemies were important in our study; they were most prevalent during July, and Hi. convergens was the species that had both the highest rates of attack and the highest richness of enemy species. This finding is relevant since Hi. convergens is considered the most important native controller of pests in crop fields, so a decrease in its abundance and/or vigor due to a high prevalence of its own natural enemies could decrease its effectiveness against economically important pests (Iperti 1999). However, it is also possible that because Hi. convergens was the most abundant ladybird we were more readily able to detect its parasitoids. To further evaluate the effect of ladybirds as biocontrol agents on insect herbivores, future studies need to consider how the parasitoid prevalence affects herbivore control; however, since it did not reach more than 10% overall, it may not interfere substantially with the desired effect of biocontrol in this region.
The parasitoid D. coccinellae had an overall rate of emergence of 7.19%. This species is cosmopolitan, and it is known to attack 72 ladybird species with variable efficiency depending on latitude and habitat type (Fei et al. 2023; Ceryngier et al. 2023). In this study, the ladybird most affected by the parasitoid was Hi. convergens. Its parasitism rate was similar to the 8% reported by Bjørnson (2008). In Italy, Coc. septempunctata, A. bipunctata, and Hi. variegata showed parasitism rates between 2.3 and 6.2% (Dindo et al. 2016). In Canada, parasitism of Col. maculata in alfalfa and maize crops was 5.9% (Firlej et al. 2005).
Recently, Ha. axyridis (exotic in Mexico) has been recognized as the second most frequently recorded host of D. coccinellae (Ceryngier et al. 2018, 2023; Romanov 2019; Romero et al. 2020). In our study, the abundance of Ha. axyridis was very low (N = 19) and none of the individuals examined showed signs of parasitism, so we will need to increase our sample size to draw any conclusions on about the parasitism by D. coccinellae in this species. In Europe, Knapp et al. (2019) reported up to 46% of Ha. axyridis parasitized by D. coccinellae, significantly higher than co-occurring native species, while in Chile, the parasitism rate was 7% (Romero et al. 2020) and in Brazil 25% (Paula et al. 2021).
The prevalence of parasitic nematodes in our sample of ladybirds was low—only 1.89% of individuals. However, this is the first report of this interaction in Mexico. These parasitic nematodes have been used as biocontrol agents for insect species (Platzer 1981), but their host specificity has not been studied thoroughly (Petersen 1985). Hippodamia convergens and P. vittigera were the species attacked by these parasites. Other studies have found higher Mermithidae infestation rates (27%) in Coc. septempunctata during the overwintering period in Turkey (Tarla 2019), and several studies in India, Uzbekistan, Poland, and Germany have found variable levels of nematode infestation in ladybirds (Rahaman et al. 2000; Mathchanov et al. 1984 reported in Tarla 2019; Ceryngier 2000; Kaiser and Nickle 1985). Since nematode parasitism causes host death, they have the potential to decrease ladybird populations and may hamper the natural biocontrol exerted by these Coleoptera in agricultural fields, but the magnitude of their effects warrants further investigation in our study sites.
Mites were the least abundant parasites in our study; however, we were limited by the number of specimens examined, since we only sampled these ectoparasites when we were able to find more than 15 individuals per species per plot (a total of 19 samples/69 specimens). Hippodamia convergens and P. vittigera were the species parasitized by adults and larvae of Coccipolipus spp. Previous studies have documented that this genus is able to parasite Ladybirdae (Coccinellini, Epilachnini and Chilocorini). Ceryngier et al (2012) reported that they feed upon Hi. convergens, Cy. sanguinea, Ha. axyridis, Coc. septempunctata, A. bipunctata, Epilachna spp., and Chilocorus spp. These mites consume hemolymph under the host’s elytra, and they are transmitted during ladybird copulation and overwintering. The most well-studied species of the genus are Coccipolipus macfarlanei and C. hippodamiae (Hajiqanbar and Joharchi 2011; Webberley et al. 2004). Since C. hippodamiae has been reported attacking Hi. convergens in the USA and Ha. axyridis in Poland and the USA (Ceryngier et al. 2012; Riddick et al. 2009; Riddick 2010), it seems the most probable species for our site. The impact of these mites on ladybird populations is variable (Riddick et al. 2009), but some investigations report female infertility and a decrease in egg hatching (Webberley et al. 2004; Rhule et al. 2010; Shaikevich et al. 2023). Indirect effects of mites related to the transmission of Wolbachia and Spiroplasma have been reported for Coccipolipu.s hippodamie (Shaikevich et al. 2023). Wolbachia is known to interfere with ladybird reproductive behavior, including parthenogenesis and causing the death of most males (Werren et al. 2008). Therefore, these parasites can be added to the factors affecting ladybird populations in our study region.
Conclusions
Our study provides information on a diversity of interactions between adult predatory ladybirds and some of their natural enemies—parasitoids, nematodes, and mites—in areas with varying degrees of disturbance in Mexico. Both ladybirds and their natural enemies were more diverse and abundant in maize agricultural fields than fallow lands and matorrals. Our results offer a first approach to the community of natural enemies of predatory ladybirds in Mexico. This information about the ecology of ladybirds of agricultural importance in the region is relevant for conservation biological control programs in agriculture, since they must consider the different ladybird mortality factors in order to be sustainable.
Data availability
All the data is provided in the tables included in the paper.
References
Almdal CD, Costamagna AC (2023) Annual crops contribute more predators than perennial habitats during an aphid outbreak. Insects 14(7):624. https://doi.org/10.3390/insects14070624
Ameixa OMCC, Soares AO, Soares AMVM, Lilleb AI (2018) Ecosystem services provided by the little things that run the world. In: Sen B (ed) Selected studies in biodiversity. InTech, London
Awad M, Piálková R, Haelewaters D, Nedvěd O (2023) Infection patterns of Harmonia axyridis (Coleoptera: Coccinellidae) by ectoparasitic microfungi and endosymbiotic bacteria. J Invertebr Pathol. https://doi.org/10.1016/j.jip.2023.1078872
Bianchi FJJA, Booij CJH, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc R Soc B 273(1595):1715–1727. https://doi.org/10.1098/rspb.2006.3530
Biddinger DJ, Weber DC, Hull LA (2009) Coccinellidae as predators of mites: Stethorini in biological control. Biol Control 5:268–283. https://doi.org/10.1016/j.biocontrol.2009.05.014
Bjørnson S (2008) Natural enemies of the convergent lady beetle, Hippodamia convergens Guérin-Méneville: their inadvertent importation and potential significance for augmentative biological control. Biol Control 44(3):305–311. https://doi.org/10.1016/j.biocontrol.2007.10.001
Brown PMJ, Roy HE (2018) Native ladybird decline caused by the invasive harlequin ladybird Harmonia axyridis: evidence from a long-term field study. Insect Conserv Divers 11(3):230–239. https://doi.org/10.1111/icad.12266
Camacho-Cervantes M, Ortega-Iturriaga A, del-Val E, (2017) From effective biocontrol agent to successful invader: the harlequin ladybird (Harmonia axyridis) as an example of good ideas that could go wrong. PeerJ 5(3):e3296. https://doi.org/10.7717/peerj.3296
Camacho-Cervantes M, Mendoza-Arroyo W, Arellano-Sanchez D, del-Val E, (2021) Exotic predators are not better biocontrol agents: the harlequin ladybird is not the most voracious in Mexico. Peer J 9:e12503. https://doi.org/10.7717/peerj.12503
Ceryngier P (2000) Overwintering of Coccinella septempunctata (Coleoptera: Coccinellidae) at different altitudes in the Karkonosze Mts, SW Poland. Eur J Entomol 97(3):323–328. https://doi.org/10.14411/eje.2000.049
Ceryngier P, Roy HE, Poland RL (2012) Natural enemies of ladybird beetles. In: Hodek I, van Emden HF, Honěk A (eds) Ecology and behaviour of the ladybird beetles (Coccinellidae). Wiley, Oxford, pp 375–443
Ceryngier P, Nedvěd O, Grez AA, Riddick EW, Roy HE et al (2018) Predators and parasitoids of the harlequin ladybird, Harmonia axyridis, in its native range and invaded areas. Biol Invasions 20:1009–1031. https://doi.org/10.1007/s10530-017-1608-9
Ceryngier P, Franz KW, Romanowski J (2023) Distribution, host range and host preferences of Dinocampus coccinellae (Hymenoptera: Braconidae): a worldwide database. Eur J Entomol 120(1):26–34. https://doi.org/10.14411/eje.2023.004
Correa ACA, Mendoza ME, López GE (2014) Análisis del cambio en la conectividad estructural del paisaje (1975–2008) de la cuenca del lago Cuitzeo, Michoacán, México. Rev Geogr Norte Gd 23:7–23. https://doi.org/10.4067/S0718-34022014000300002
Crawley MJ (2012) The R book, 2nd edn. Wiley, Hoboken
Crous PW, Osieck ER, Jurjevi Ž, Boers J et al (2021) Fungal planet description sheets: 1284–1382. Persoonia 47:178–374. https://doi.org/10.3767/persoonia.2021.47.06
de Groot MD, Haelewaters D (2022) Double infections of the invasive ladybird Harmonia axyridis. Front Ecol Evol 10:756972. https://doi.org/10.3389/fevo.2022.756972
Dheilly NM, Maure F, Ravallec M, Galinier R, Doyon J, Duval D, Leger L, Volkoff A-N, Missé D, Nidelet S, Demolombe V, Brodeur J, Gourbal B, Thomas F, Mitta G (2015) Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behavior manipulation. Proc Biol Sci 282:20142773. https://doi.org/10.1098/rspb.2014.2773
Dindo ML, Francati S, Lanzoni A, di Vitantonio C, Marchetti E, Burgio G, Maini S (2016) Interactions between the multicolored Asian lady beetle Harmonia axyridis and the parasitoid Dinocampus coccinellae. Insects 7(4):67. https://doi.org/10.3390/insects7040067
Escalona HE, Zwick A, Li HS, Li JH, Wang XM, Pang H, Hartley D, Jermiin LS, Nedved O, Misof B (2017) Molecular phylogeny reveals food plasticity in the evolution of true ladybird beetles (Coleoptera: Coccinellidae: Coccinellini). BMC Evol Biol 17:151. https://doi.org/10.1186/s12862-017-1002-3
Fei M, Gols R, Harvey JA (2023) The biology and ecology of parasitoid wasp of predatory arthropods. Annu Rev Entomol 68:109–128. https://doi.org/10.1146/annurev-ento-120120-111607
Firlej A, Boinvin G, Lucas E, Codere D (2005) First report of Harmonia axyridis Pallas being attacked by Dinocampus coccinellae Schrank in Canada. Biol Invasions 7(4):553–556. https://doi.org/10.1007/s10530-004-5848-0
Fortoul-Diaz JV, Huerta- de la Peña A, Lomeli-Flores JR, Hernández-Salgado JH, Pérez-Magaña A (2020) Fluctuación poblacional de Melanaphis sacchari (Zehntner) e identificación de sus depredadores en sorgo con manejo tradicional en Puebla, México. Southwest Entomol 45(2):553–562. https://doi.org/10.3958/059.045.0223
Gardiner MM, Landis DA, Gratton C, DiFonzo CD, O’Neal M, Chacón JM, Wayo MT, Schmidt NP, Mueller EE, Heimpel GE (2009) Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecol Appl 19(1):143–154. https://doi.org/10.1890/07-1265.1
Giorgi JA, Vandenberg NJ, McHugh JV, Forrester JA, Slipinski SA, Miller KB, Shapiro LR, Whiting MF (2009) The evolution of food preferences in Coccinellidae. Biol Control 51:215–231. https://doi.org/10.1016/j.biocontrol.2009.05.019
Grez AA, Rand TA, Zaviezo T, Castillo-Serey F (2013) Land use intensification differentially benefits alien over native predators in agricultural landscape mosaics. Divers Distrib 19(7):749–759. https://doi.org/10.1111/ddi.12027
Grez AA, Zaviezo T, Gardiner MM, Alaniz AJ (2019) Urbanization filters coccinellids composition and functional trait distributions in green spaces across greater Santiago, Chile. Urban for Urban Green 38:337–345. https://doi.org/10.1016/j.ufug.2019.01.002
Grez AA, Zaviezo T, Casanoves F, Oberti R, Pliscoff P (2021) The positive association between natural vegetation, native coccinellids and functional diversity of aphidophagous coccinellid communities in alfalfa. Insect Cons Div 14(4):464–475. https://doi.org/10.1111/icad.12473
Haelewaters D, De Kesel A (2020) Checklist of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands, including Hesperomyces halyziae and Laboulbenia quarantenae spp. nov. MycoKeys 71:23–86. https://doi.org/10.3897/mycokeys.71.53421
Haelewaters D, Zhao SY, Clusella-Trullas S et al (2017) Parasites of Harmonia axyridis: current research and perspectives. Biocontrol 62:355–371. https://doi.org/10.1007/s10526-016-9766-8
Haelewaters D, De Kesel A, Pfister DH (2018) Integrative taxonomy reveals hidden species within a common fungal parasite of ladybirds. Sci Rep 8(1):15966. https://doi.org/10.1038/s41598-018-34319-5
Haelewaters D, Hiller T, Kemp EA, van Wielink PS, Shapiro-llan DI, Aime MC, Nedvěd O, Pfister DH, Cottrell TE (2020) Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi. PeerJ 8:e10110. https://doi.org/10.7717/peerj.10110
Haelewaters D, Blackwell M, Pfister DH (2021) Laboulbeniomycetes: intimate fungal associates of arthropods. Annu Rev Entomol 66:257–276. https://doi.org/10.1146/annurev-ento-013020-013553
Haelewaters D, Van Caenegem W, De Kesel A (2022) Hesperomyces harmoniae, a new name for a common ectoparasitic fungus on the invasive alien ladybird Harmonia axyridis. SYDOWIA 75:53–74. https://doi.org/10.12905/0380.sydowia75-2022-0053
Hajiqanbar H, Joharchi O (2011) World distribution and host range of Podapolipoides spp. (Acari: Heterostigmatina: Podapolipidae) with the description of a new species. Syst Parasitol 78(2):151–162. https://doi.org/10.1007/s11230-010-9284-5
Hodek I, Honěk A (2009) Scale insects, mealybugs, whiteflies and psyllids (Hemiptera, Sternorrhyncha) as prey of ladybirds. Biol Control 51(2):232–243. https://doi.org/10.1016/j.biocontrol.2009.05.018
Holecová M, Zach P, Hollá K, Šebestová M, Klesniaková M, Šestáková A, Honěk A, Nedvěd O, Parák M, Martinková Z, Holec J, Viglášová S, Brown PMJ, Roy HE, Kulfan J (2018) Overwintering of ladybirds (Coleoptera: Coccinellidae) on Scots pine in Central Europe. Eur J Entomol 115:658–667. https://doi.org/10.14411/eje.2018.065
Honěk A, Dixon AF, Soares AO, Skuhrovec J, Martinkova Z (2017) Spatial and temporal changes in the abundance and composition of ladybird (Coleoptera: Coccinellidae) communities. Curr Opin Insect Sci 20:61–67. https://doi.org/10.1016/j.cois.2017.04.001
Husband RW (1972) A new genus and species of mites (Acarina: Podapolipidae) associated with the Coccinellid Cycloneda sanguinea. Ann Entomol Soc Am 65(5):1099–1104
INEGI (2020) Cuenca hidrológica Lago de Cuitzeo. Humedales. Informe técnico. https://www.inegi.org.mx/contenidos/productos/prod_serv/contenidos/espanol/bvinegi/productos/nueva_estruc/702825197094.pdf Accessed December 2023
Iperti G (1999) Biodiversity of predaceous Coccinellidae in relation to bioindication and economic importance. Agric Ecosyste Environ 74(1–3):323–342. https://doi.org/10.1016/S0167-8809(99)00041-9
Kaiser VH, Nickle WR (1985) Mermithiden (Mermithidae, Nematoda) parasitieren Marienkafer (Coccinella septempunctata L.) in der Steiermark. Mitt Naturwiss Ver Steiermark 115:115–118
Knapp M, Řeřicha M, Maršíková S, Harabiš F, Kadlec T, Nedvěd O, Tender T (2019) Invasive host caught up with a native parasitoid: field data reveal high parasitism of Harmonia axyridis by Dinocampus coccinellae in Central Europe. Biol Inv 21(9):2795–2802. https://doi.org/10.1007/s10530-019-02027-4
Krantz GW, Walter DE (2009) A manual of acarology, 3er edn. Texas Tech University Press, Lubbock
Labrie G, Coderre D, Lucas É (2008) Overwintering strategy of multicolored Asian lady beetle (Coleoptera: Coccinellidae): cold-free space as a factor of invasive success. Ann Entomol Soc Am 101(5):860–866. https://doi.org/10.1603/0013-8746
Landis DA, Gardiner MM, Van Der Werf W, Swinton SM (2008) Increasing corn for biofuel production reduces biocontrol services in agricultural landscapes. Proc Natl Acad Sci USA 105(51):20552–20557. https://doi.org/10.1073/pnas.0804951106
Li H, Shu X, Meng L, Zhou X, Obrycki JJ, Li B (2021) Prevalence of maternally-inherited bacteria in native and invasive populations of the harlequin ladybird beetle Harmonia axyridis. Biol Invasions 23:1461–1471. https://doi.org/10.1007/s10530-020-02451-x
López-Piña G, Ponce-Saavedra J (2017) Coccinélidos (Coleoptera: Coccinellidae) del Estado de Michoacán, México. Biologicas 19(2):16–27
Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56(4):311–323. https://doi.org/10.1641/0006-3568(2006)56[311:tevoes]2.0.co;2
Lourdes EY, Van Lun LL, Izwan-Anas N, Mohamed Dawood M, Sofian-Azirun M, Takaoka H, Ya’cob Z (2023) Occurrence of five distinct clades of mermithid nematodes (Nematoda: Mermithidae) infecting black fly larvae (Diptera: Simuliidae) in tropical streams in Malaysia. Parasitol Int 94:102733. https://doi.org/10.1016/j.parint.2023.102733
McDaniel B, Morrill W (1969) A new species of Tetrapolipus from Hippodamia convergens from South Dakota (Acarina: Podopolipidae). Ann Entomol Soc Am 62(6):1465–1468. https://doi.org/10.1093/aesa/62.6.1465
Miller CR, Barton BT, Zhu L, Radeloff VC, Oliver KM, Harmon JP, Ives AR (2017) Combined effects of night warming and light pollution on predator–prey interactions. Proc Roy Acad Sci B 284:1–8. https://doi.org/10.1098/rspb.2017.1195
Morteo-Montiel S, Simms SR, Porter-Bolland L, Bonilla-Moheno M (2021) Does the simplification of activity systems produce landscape homogenization? Environ Dev Sustain 23:5695–5714. https://doi.org/10.1007/s10668-020-00839-2
Nickle WR (1972) A contribution to our knowledge of the Mermithidae (Nematoda). J Nematol 4(2):113–146
Obrycki JJ, Harwood JD, Kring TJ, O´ Neil RJ, (2009) Aphidophagy by Coccinellidae: application of biological control in agroecosystems. Biol Control 51(2):244–254. https://doi.org/10.1016/j.biocontrol2009.05.009
Paula DP, Togni PHB, Costa VA, Souza LM, Sousa AATC, Tostes GM, Pires CSS, AndowDA, (2021) Scrutinizing the enemy release hypothesis: population effects of parasitoids on Harmonia axyridis and local host coccinellids in Brazil. BioControl 66:71–82. https://doi.org/10.1007/s10526-020-10041-y
Petersen JJ (1985) Nematodes as biological control agents: part I. Mermithidae. In: Baker JR, Muller R (eds) Advances in parasitology. Elsevier, England, pp 307–344
Platzer EG (1981) Biological control of mosquitoes with Mermithids. J Nematol 13(3):257–262
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org/
Rahaman PF, Sharma SB, Wightman JA (2000) A review of insect-parasitic nematode research in India. Int J Pest Manag 46:19–28. https://doi.org/10.1080/096708700227543
Ramaraju K, Poorani J (2012) A new species of Coccipolipus (Acari: Podapolipidae) parasitic on the giant coccinellid beetle from India. Int J Acarol 38(4):290–296. https://doi.org/10.1080/01647954.2011.651156
Ramzan Z, Khursheed S (2023) Predatory potential and functional response of Coccinella undecimpunctata Linnaeus (Coleoptera: Coccinellidae) on Brevicoryne brassicae (Linnaeus) (Homoptera: Aprhididae). Int J Pest Manag. https://doi.org/10.1080/09670874.2023.2234330
Rhule EL, Majerus MEN, Jiggins FM, Ware RL (2010) Potential role of the sexually transmitted mite Coccipolipus hippodamiae in controlling populations of the invasive ladybird Harmonia axyridis. Biol Control 53(2):243–247. https://doi.org/10.1016/j.biocontrol.2009.12.006
Riddick EW (2010) Ectoparasitic mite and fungus on an invasive lady beetle: parasite coexistence and influence on host survival. Bull Insectology 63(1):13–20
Riddick EW, Cottrell TE, Kidd KA (2009) Natural enemies of the Coccinellidae: parasites, pathogens, and parasitoids. Biol Control 51(2):306–312. https://doi.org/10.1016/j.biocontrol.2009.05.008
Rodríguez LA, Arredondo HC, Williams T, Barrera JF (2015) Pasado, presente y perspectivas del control biológico en México. In: Arredondo HC, Rodríguez del Bosque LA. Casos de Control Biológico en México, Vol 2. 1er edn. Editorial del Colegio de Postgraduados, Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Universidad Autónoma Cha**o. Guadalajara, Jalisco, Mexico. pp 17–28
Rodríguez-Del-Bosque LA, Rodríguez-Vélez B, Sarmiento-Cordero MA, Arredondo-Bernal HC (2018) Natural enemies of Melanaphis sacchari on Grain Sorghum in Northeastern Mexico. Southwest Entomol 43(1):277–279. https://doi.org/10.3958/059.043.0103
Romanov DA (2019) Parasitoids of the harlequin ladybeetle Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae). Russ J Biol Invasions 10:52–67. https://doi.org/10.1134/S2075111719010144
Romero V, Zaviezo T, Grez AA (2020) The invasive coccinellids Harmonia axyridis (Coleoptera: Coccinellidae) is a less suitable host for parasitism than resident species. Int J Agric Nat Resour 47(3):312–323. https://doi.org/10.7764/ijanr.v47i3.2239
Roy HE, Brown PMJ, Rothery P, Ware RL, Majerus MEN (2008) Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellids: Harmonia axyridis Coccinella Septempunctata and Adalia Bipunctata. Biocontrol 53(1):256–276. https://doi.org/10.1007/s10526-007-9122-0
Roy HE, Rhule E, Harding S, Handley LJL, Poland RL, Riddick EW et al (2011) Living with the enemy: parasites and pathogens of the ladybird Harmonia axyridis. Biocontrol 56:663–679. https://doi.org/10.1007/s10526-011-9387-1
Rusconi JM, Bárbara Defea BS, Montes MM, Achinelly MF (2020) First record of Mermithid nematodes, parasitizing leafhoppers in South America. Caldasia 42(1):147–149. https://doi.org/10.15446/caldasia.v42n1.73601
Sethuraman A, Tovar A, Welch W, Dettmers R, Arce C, Skaggs T, Rothenberg A, Saisho R, Summerhays B, Cartmill R, Grenier C, Vasquez Y, Vansant H, Obrycki J (2022) Genome of the parasitoid wasp Dinocampus coccinellae reveals extensive duplications, accelerated evolution, and independent origins of the thelytokous parthenogeny and solitary behavior. G3 Genes Genomes Genetics 12(3):001. https://doi.org/10.1093/g3journal/jkac001
Shaikevich EV, Gorbacheva AA, Romanov DA (2023) Ectoparasitic mites: vectors of bacterial symbionts among insects. Biol Bull Russ Acad Sci 50:338–347. https://doi.org/10.1134/S1062359023700231
Shrestha RB, Parajulee MN (2013) Potential cotton aphid, Aphis gossypii, population suppression by arthropod predators in upland cotton. Ins Sci 20(6):778–788. https://doi.org/10.1111/j.1744-7917.2012.01583.x
Silva RB, Cruz I, Figueiredo MLC, Pereira AG, Penteado-Dias AM (2012) Occurrence and biology of Dinocampus coccinellae (Schrank, 1802) (Hymenoptera; Braconidae: Euphorinae) parasitising different species of Coccinellidae (Coleoptera) in Neotropical region. Braz J Biol 72(1):215–219. https://doi.org/10.1590/S1519-69842012000100027
Sloggett JJ (2021) Aphidophagous ladybirds (Coleoptera: Coccinellidae) and climate change: a review. Insect Conserv Div 14(6):709–722. https://doi.org/10.1111/icad.12527
Soares AO, Haelewaters D, Ameixa OMCC, Borges I, Brown PMJ, Cardoso P, de Groot MD, Evans EW, Grez AA, Hochkirch A, Holecová M, Honek A, Kulfan J, Liellobo AI, Martinkova Z, Nedved O, Omkar RHR, Saxena S, Shadilya A, Sentis A, Skuhrovec J, Viglasová S, Zach P, Zaviezo T, Losey JE (2023) A roadmap for ladybird conservation and recovery. Conserv Biol 37:e13965. https://doi.org/10.1111/cobi.13965
Sun B, Li F, He X, Cao F, Bandason E, Shapiro-Ilan D, Ruan W, Wu S (2020) First report of Ovomermis sinensis (Nematoda: Mermithidae) parasitizing fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae) in China. J Nematol 52:1–7. https://doi.org/10.21307/jofnem-2020-050
Tarla G (2019) Hexamermis (Nematoda: Mermithidae) Infecting Coccinella septempunctata (Coleoptera: Coccinellidae) in overwintering areas in Turkey. Entomol News 129(1):55–62. https://doi.org/10.3157/021.129.0108
van Caenegem W, Ceryngier P, Romanowski J, Pfister DH, Haelewaters D (2023) Hesperomyces (Fungi, Ascomycota) associated with Hyperaspis ladybirds (Coleoptera, Coccinellidae): rethinking host specificity. Front Fungal Biol 3:1040102. https://doi.org/10.3389/ffunb.2022.1040102
van Lenteren JC, Bolckmans K, Kohl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol 63(1):39–59. https://doi.org/10.1007/s10526-017-9801-4
Watanabe S, Tsunashima A, Itoyama K, Shinya R (2021) Survey of mermithid nematodes (Mermithida: Mermithidae) infecting fruit-piercing stink bugs (Hemiptera: Pentatomidae) in Japan. Appl Entomol Zool 56:27–39. https://doi.org/10.1007/s13355-020-00705-7
Webberley KM, Hurst GDD, Husband RW, Schelenburg JHGVD, Sloggett JJ, Isham V, Buszko J, Majerus MEN (2004) Host reproduction and a sexually transmitted disease: causes and consequences of Coccipolipus hippodamiae distribution on coccinellid beetles. J Anim Ecol 73(1):1–10. https://doi.org/10.1111/j.1365-2656.2004.00769.x
Werren J, Baldo L, Clark M (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751. https://doi.org/10.1038/nrmicro1969
Wharton RA, Marsh PM, Sharkey MJ (1997) Manual of the new World Genera of the family Braconidae (Hymenoptera). R. A. Wharton, P. M. Marsh, & M. J. Sharkey, (Eds) (1st ed). The international society of Hymenopterists. Washington, DC, USA
Acknowledgements
W. Mendoza acknowledges the grant provided by Consejo Nacional de Humanidades Ciencia y Tecnología México (Conahcyt) to study her Master’s Degree, to the Posgrado en Ciencias Biológicas of Universdad Nacional Autónoma de México, and to Dirección General de Asuntos del Personal Académico-Papiit project BG 200720. Parasitoid identification was corroborated by Alejandro Zaldivar at the Colección Nacional de Insectos, Instituto de Biología -UNAM; molecular identification of the nematode was performed by Uriel Garduño, Colección Nacional de Helmintos en el Instituto de Biología -UNAM; Acari identification was corroborated by Griselda Montiel Parra at the Colección Nacional de Ácaros, Instituto de Biología -UNAM.
Funding
Funding was provided by Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México (BG 200720) to Wendy Mendoza-Arroyo.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant conflicts of interest to report.
Additional information
Handling Editor: Danny Haelewaters.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Mendoza-Arroyo, W., del-Val, E. Ladybird predators in natural and agricultural landscapes in Mexico: diversity and parasitism. Arthropod-Plant Interactions (2024). https://doi.org/10.1007/s11829-024-10075-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11829-024-10075-4