https://orcid.org/0009-0001-9520-5986
Figures
Abstract
This study examines the community composition and structure of psyllophagous ladybirds in a tropical environment, focusing on their interactions with psyllids as a food resource. It investigates the effects of prey availability and landscape composition on the structure of all ladybird species associated with psyllids and on the presence and abundance of species whose life cycles depend on psyllids. Sampling was conducted in Reunion island on two psyllid-infested plant species, Leucaena leucocephala and Acacia heterophylla. Ladybirds and psyllids were regularly collected during two years using a thermal aspirator, and visual inspection was conducted at eleven sites visited monthly. In this study, 16 ladybird species were identified, and only juveniles from Coccinella septempunctata, Exochomus laeviusculus, and Olla v-nigrum were frequently present, suggesting they can complete their biological cycle on psyllids. The structure of psyllophagous ladybird communities in a tropical environment is driven by the psyllid host plant and the monthly average temperature. When studied separately, food resources or landscape variables did not affect significantly the communities. The distribution of Coccinella septempunctata is limited to high elevations, where it is recognized as an aphid-eating species, mainly in its juvenile form. Conversely, at low elevation, we encountered juvenile individuals of the generalist species Exochomus laeviusculus and the specialist species Olla v-nigrum. The presence and abundance of the generalist was positively influenced by the landscape and the presence of the specialist positively by prey abundance only.
Citation: Baujeu M, Moquet L, Chiroleu F, Becker-Scarpitta A, Reynaud B (2025) The impact of landscape and prey on psyllophagous ladybird communities in a tropical environment. PLoS ONE 20(4): e0320898. https://doi.org/10.1371/journal.pone.0320898
Editor: Ramzi Mansour, University of Carthage, TUNISIA
Received: August 22, 2024; Accepted: February 27, 2025; Published: April 11, 2025
Copyright: © 2025 Baujeu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All data will be available at : https://doi.org/10.18167/DVN1/WLU1UR.
Funding: This work is included in the CREME project “Conservation et Restauration des Espèces et des Milieux Endémiques” run by the University of La Réunion and co-financed by the European Regional Development Fund (ERDF) and the “Region Réunion” (N° GURDTI/20201012-0022961) M. Baujeu is a PHD student and beneficed a doctoral allocation co-financed by the European Regional Development Fund (ERDF) and the “Region Réunion” (N°DIRED/20210154). L. Moquet, F. Chiroleu and A. Becker-Scarpitta were co-financed by European Agricultural Fund for Regional Development (EAFRD) and the “Region Réunion”.
Competing interests: The authors have declared that no competing interests exist.
Introduction
An ecological community is a group of species coexisting in the same habitat and interacting with one another around shared resources [1]. Understanding the dynamics of ecological communities is a cornerstone of ecology. Communities are influenced by a range of abiotic factors including climate [2–6], land type and cover [2,7], resource availability [8,9], and geographical characteristics [10]. These factors collectively shape community composition, structure, and function, providing insights into species interactions, biodiversity, and ecosystem dynamics [1,11].
Research on ladybird communities (Coccinellidae) has significantly contributed to our understanding of these dynamics and has tested various concepts in community ecology [12]. The Coccinellidae family encompasses about 6000 species across 360 genera [13,14]. While most ladybirds are predators of other arthropods [15,16], some species are phytophagous or mycophagous [17]. A distinctive behavior of predatory ladybirds is their tendency to aggregate around abundant food resources [18–23], which is important for understanding their community structure. Whether or not the species feed obligatorily on prey, this aggregation creates interaction dynamics within the community, where competition and predation collectively shape the organization of all species present.
In temperate regions, prey availability is the main factor explaining the composition of aphidophagous ladybird communities at the habitat scale [24–27]. According to Honek & Evans, 2012 [28] they rely on different prey types: (i) essential prey, crucial for reproduction and larval development; (ii) accepted prey, a secondary less favourable food resource; and (iii) alternative prey, which sustains survival in scarcity. Aphidophagous ladybird communities include mobile generalist adults and sedentary specialist larvae reliant on specific prey. Prey abundance affects the presence of adults, female oviposition choices, and larval abundance [29,30]. Smaller ladybird species can persist at lower prey densities, while larger species require higher abundances to sustain their populations [31]. Additionally, ladybird adults possess prey detection thresholds, responding only when prey density reaches a certain level, which influences their distribution and aggregation patterns within habitats [32].
Landscape characteristics, including diversity, fragmentation, and the availability of host plants, play a role in structuring aphidophagous ladybird communities. Diverse landscapes, which offer a range of prey and habitats, particularly benefit generalist species that can exploit various resources due to their dietary flexibility [33]. In contrast, landscape fragmentation creates barriers that restrict movement and limit habitat access, disproportionately affecting species with low dispersal capacities, often smaller in size [34,35]. Finally, the availability of host plants for larvae directly influences the distribution of specialist species whose life cycles are closely tied to psyllids. These host plants support communities by providing breeding sites and a stable food resource for juvenile stages [27].
Most studies on ladybird communities have focused on aphidophagous species in temperate continental agricultural systems [7,23,33,36–38] but there is limited understanding of psyllophagous species. Psyllids, while less common prey, are essential for some Coccinellini [15]. Giorgi et al. (2009) [39] identified only three of 62 ladybird species as having psyllids as essential prey. Some studies confirm psyllids as essential for certain species [40–43]. Most research on psyllophagous ladybirds has been observational or correlational [41,43]. Nevertheless, many studies have explored the introduction of ladybirds to control psyllid pests [44–53]. Psyllids are highly specific to host plants, with fewer than 25 species being significant agricultural pests [54,55]. They feed on phloem, xylem, and parenchyma [56,57], sometimes transmitting pathogens such as Candidatus Liberibacter, which causes citrus greening disease [58,59].
Our study investigates the composition of psyllid-feeding ladybird communities on Réunion Island in the southwest Indian Ocean. The coexistence of obligatory or occasionally psyllophagous and non-psyllophagous species within the same micro-habitat leads to distinct interaction dynamics, where competition among psyllid feeders and predation by non-feeders collectively shape the structure of the ladybird community.
We aim to: (i) identify all species interacting with psyllid-feeding ladybirds, whether they consume psyllids occasionally, as a primary resource, or play other ecological roles within psyllophagous communities; (ii) investigate how prey availability influences the structure of psyllophagous ladybird communities, depending on their traits of dietary specificity and body size and (iii) explore how landscape characteristics shape the structure of psyllophagous ladybird communities, with a focus on how dietary specificity and body size traits influence species’ responses
We propose the following hypotheses: (i) Psyllophagous ladybird communities are primarily composed of generalist adults, with a minority of specialist species, including larvae, that depend on psyllids as essential prey (ii) increased psyllid abundance is expected to enhance the density of psyllophagous ladybird populations, particularly for specialist species whose larvae and adults rely on psyllids as a primary resource (iii) Diverse landscapes will favor generalist species due to increased prey diversity, availability of host plants is expected to enhance specialist species and landscape fragmentation is expected to disadvantage smaller species due to their limited dispersal capabilities.
Materials and methods
Study context
In the 1980s, widespread infestations of the psyllid Heteropsylla cubana Crawford, 1914 (Hemiptera: Psyllidae), severely impacted Leucaena leucocephala (Lam.) de Wit in many regions, causing extensive defoliation and threatening the viability of Leucaena as a key resource in agroforestry and grazing systems [60–62]. In response, biological control programs were implemented globally, including in La Réunion, where predatory ladybirds such as Olla v-nigrum (Mulsant, 1866) and Curinus coeruleus (Mulsant, 1850) were introduced to manage psyllid populations [63,64]. Currently, the IUCN classifies this plant species as one of the world’s 100 most invasive exotic plants. It can be found in Reunion island at elevations of between 0 and 400 meters.
Today, a new psyllid invasion poses a similar threat to an endemic species from La Réunion, Acacia heterophylla Willd., which is experiencing significant ecological pressure from the invasive psyllid Acizzia uncatoides (Ferris & Klyver, 1932). Since its detection in La Réunion in 2006, A. uncatoides has caused severe damage to Acacia heterophylla resulting in increased tree mortality and ecosystem disruption [65]. This recurring challenge raises questions about the role of biological control in managing invasive psyllid populations on the island. Tamarind Forests extend from an elevation of 1400 to 2000 m [66,67].
By studying these two host plants, Leucaena leucocephala and Acacia heterophylla, this research bridges past and future biological control strategies, examining how historical interventions can inform current approaches to manage psyllid invasions and protect La Réunion’s native flora.
Site selection
All sampling was carried out in Reunion island, a French oceanic island located in the south-western part of the Indian Ocean (long: 55°30’; lat: 21°11) (Fig 1). Reunion island is characterized by abundant rainfall, especially during the warm season. Rainfall distribution varies significantly across the island, with the south-eastern region receiving up to eight times more precipitation than the north-western region. Additionally, the island’s coastal and low-elevation areas typically experience lower levels of rainfall compared to its central, mountainous regions (Météo-France, 2020). Temperatures vary along the elevational gradient and across the seasons. At low elevations, on the coast, average temperatures vary between 20°C and 30°C during the wet season. In the dry season, temperatures can drop to 15°C at night. Temperatures are lower in mountainous regions and temperatures close to 0°C have been recorded at the highest peaks. Annual solar radiation intensity ranges from 1400–2500 h and can reach 2900 h at elevations below 400 m [68].
Elevation data from RGE ALTI® (source: IGN, 2023).
Coccinellidae sampling design has been based on the psyllid host plants’s presence, and we specifically targeted two heavily infested species: Leucaena leucocephala and Acacia heterophylla.
Eleven sites were sampled (Fig 1, source: [69]): six at low elevations corresponding to the distribution area of L. leucocephala and five at high elevations corresponding to the distribution area of A. heterophylla. The sites were chosen based on accessibility and the high availability of acacia and leucaena host plants within an approximate area of 50 m2 to facilitate sampling. All the sampling sites are located on the less humid west coast, which reduces the likelihood of frequent psyllid leaching.
Psyllids and ladybird counts
Each site was sampled between 5 and 10 times (Table 1) between December 2020 and April 2022 during the hot rainy season. For each sampling (=each visit to a site on a given date), monthly average temperature, monthly cumulated precipitation and monthly average solar radiation intensity were calculated over the thirty days preceding the sampling using data from the Smart IS database (©CIRAD, 2022, https://smartis.re/).
A Garden Vacuum (Garden Vacuum STIHL® D-71336 Waiblingen), coupled with a fine mesh cloth, was used to collect the samples by vacuuming for one minute. Each sampling involved collecting one sample from each of ten unique trees, resulting in ten samples per sampling session. Using this method, we were able to quantify the psyllid population based on the presence of adult psyllids. Each sample was complemented with a hand collecting of the ladybird larvae and adults’ ladybirds found on the same branches previously sampled with the GVAC. This made ladybird sampling more effective and provided an accurate estimate of ladybird abundance and species richness.
We counted the ladybird larvae and adults, as well as adult psyllids. Ladybird larvae and adults were identified in the laboratory, using the keys provided by Chazeau et al. 1974 [70], supplemented by Quilici et al. 2003 [71], Poussereau et al. 2018 [72] and Magro et al. 2020 [73].
The pupal stage is immobile; therefore, the presence of pupae is directly linked to the presence of larvae. For our analyses, we added up the number of larvae and nymphs per tree to give us the number of “juveniles”.
We crosschecked our identifications for the juvenile ladybird stages. This involved randomly selecting 10% of the individuals for molecular identification by sequencing the traditional cytochrome oxidase 1 using LCO/HCO primers [74]. The sequences obtained were processed with Geneous® software v 10.2.6 (https://www.geneious.com) and compared with BLAST (Basic Local Alignment Search Tool), using the GenBank® reference database. The identifications were validated for all juveniles with a pair-wise sequence identity greater than 97%.
Psyllid adults were counted one by one when their number did not exceed 1000 individuals per sample. When samples had more than 1000 individuals, we separated the psyllid adults and juveniles using a filtration and sieving system (mesh size = 1 mm). The psyllid adults recovered in this way were freeze dried (ALPHA® 1-2 LDplus) for 24 hours and then weighed using a precision balance (Cubis® MCE125P-2S00-A). The number of psyllids was estimated by dividing the mass of psyllids by the average mass of one freeze-dried psyllid, previously determined from 1000 individuals (mH.Cubana = 0.077 ± 0.012 mg; mA.uncatoides = 0.111 ± 0.020 mg).
Measures of landscape composition
We studied the landscape using QGIS® mapping software (version 3.22.7-Białowieża).
A geographical reference point was positioned at the centre of each site. The coordinates were read using a handheld GPS (Garmin Forerunner® 745). The land use map created by CIRAD [75] provided raw data (crop type, natural vegetation type, building type/inert surface). This allowed us to calculate the diversity of vegetation cover index for a radius of 1 km [23,33] around the geographical reference points using Simpson’s index, which considers habitat richness and landscape homogeneity. The equation for Simpson’s index is as follows:
pi is the proportion of habitat in the ith land use category, based on 29 landscape categories (refer to Supplementary S1 Table. and S2 Fig. Data for details).
Using the same radii around the geographical reference points, we also counted the number of different landscape patches to determine landscape fragmentation.
Statistical analysis
All data processing and statistical analysis were carried out using R (R Core Team, 2023, version 4.2.3).
For every statistical analysis conducted, with the exception for canonical multivariate analysis, we opted to analyze data from psyllid and ladybird sampling on A. heterophylla and L. leucocephala separately, mainly because of the significant difference between community composition and ecosystem structure. Additionally, individuals collected using both the GVAC method and manual collection from the same tree were combined for analysis.
Ladybird community structure.
For the community analysis, given the different numbers of trees sampled per survey, we averaged numbers of ladybird juveniles and adults per species and the psyllid abundance per survey -i.e., the numbers of individual collected using the thermal aspirator. To preserve the quality of the information, species abundance data were transformed into the Hellinger distance matrix following the approach presented byLegendre et al. (2001)[76]. Environmental variables were standardized.
To test the relationships between ladybird community composition and the landscape (i.e., Simpson’s Landscape Diversity Index, fragmentation and psyllid host plant cover), the climate (i.e., the monthly average temperature, rainfall and solar intensity radiation over the thirty days prior to sampling) and the prey abundance we performed a canonical analysis using a redundancy analysis, with the function rda from the R package ‘vegan’ v2.6.4 [77]. The RDA including ladybird communities associated with Acacia heterophylla and Leucaena leucocephala. The global model (drived with all data) included the psyllid host plant (A. heterophylla or L. leucocephala) as an explanatory variable to account for its influence on community structure.
To separate the effect of site variables (Simpson’s Landscape Diversity Index, fragmentation and psyllid host plant cover) from that of the other explanatory variables on community composition, in order to control pseudo-replication effects, we build a partial RDA by setting all the parameters relating to the site as a condition factor in the model.
We conducted three independent models: one model with all data including the psyllid species as an unconstrained variable only for this model; two models with a subset of the data including only the community associated with only one host species: A. heterophylla; or L. leucocephala. All three models followed the same structure:
The final model followed this structure:
The models were tested using anova function with 999 permutations. The adjusted-R2 will quantify the variance explained by all environmental variables.
Beta diversity was analyzed separately using the betadisper function, which assesses the dispersion of species composition across sampling sites. This analysis compared the variability in species composition between communities associated with the two host plants, independent of the RDA model.
Presence and abundance of ladybirds whose life cycle depends on psyllids.
To assess the effect of landscape (Simpson’s Landscape Diversity Index, fragmentation and psyllid host plant cover), climate (monthly average temperature, monthly cumulated rainfall and monthly average solar intensity radiation over the thirty days prior to sampling), and prey resource (number of psyllids collected in one minute using the GVAC) on the presence and abundance of ladybird adults and juveniles whose life cycle depends on psyllids, we used a generalized linear mixed-effects model (GLMM) through the ‘glmer’ function from the ‘lme4’ R package v1.1.35 [78]. GLMM is well-suited for analysing complex datasets where the response variable does not follow a normal distribution and may exhibit non-constant variance, discrete outcomes or other non-Gaussian characteristics. Moreover, we collected our samples several times at the same sites, i.e., our data was not independent. Therefore, careful analysis was essential to avoid any criticism of an artificial increase in degrees of freedom (i.e., so-called pseudo-replication) [79]. Pseudo-replication refers to the incorrect analysis or interpretation of replications that are not statistically independent, such as repeated observation of the same subjects (in our case, populations) [80]. However, GLMMs (generalized linear mixed models) are capable of handling hierarchically structured and unbalanced datasets, similar to ours, and effectively solving the statistical problem of pseudo-replication [79,81]. Specifically, we included random intercepts for both the site identifier and the sampling event. By incorporating random effects, we enhance the robustness of our statistical model, by accounting for the unique characteristics associated with each site and each sampling event in our study. This comprehensive framework provides a more accurate representation of the underlying data structure and strengthens the validity of our statistical inferences.
Therefore, for this analysis, we chose to focus on just three species found in their juvenile stages on psyllid colonies: Coccinella septempunctata Linnaeus, 1758 on A. heterophylla; and Exochomus laeviusculus Weise, 1909 and Olla v-nigrum (Mulsant, 1866) on L. leucocephala. Given the wide range of values, we log-transformed the number of psyllids collected per minute to help models convergence. Presence/absence was analysed for each development stage (adult and juveniles), using nested GLMER assuming binomial distribution with species background and landscape, climatic and food resource variables as fixed factors, the statement as a nesting factor, and site sampling as a random factor. The abundance of adults and juveniles for the 3 species were analysed by nested GLMER with Poisson distribution and the same explanatory variables. The significance of each specified fixed effect in the model was assessed using “Type II Tests of Fixed Effects”. We checked the “normality” of residuals, homogeneity of variance and independence of residuals.
Results
Global ladybird community structure
A total of 4259 adult and 1539 juvenile ladybirds were collected. Sixteen species were identified, including 15 at the adult stage and 6 at the larval stage (Fig 2).
The colour gradient from red to beige indicates a low to high relative abundance. Images provided by Antoine Franck, CIRAD.
Across the study design, Exochomus laeviusculus, Olla v-nigrum and Coccinella septempunctata were the three most abundant species.
The beta diversity of the two sub-communities is significantly different, with a larger difference in composition for sites associated with Acacia heterophylla compared to Leucaena leucocephala (average distance to median group Acacia heterophylla = 0.634; group Leucaena leucocephala = 0.262, betadiper test: F-value = 41.676, Df = 1, P-value < 0.001). This result is supported by Fig 3, showing that the sub-community of psyllid ladybirds generally found at high elevations associated with A. heterophylla (in red in the Fig 3) has a broader ellipse compared to the sub-community of psyllid ladybirds generally found at low elevations associated with L. leucocephala (in brown in the Fig 3).
Ellipses show 95% confidence limits for each plant host group: Acacia heterophylla (red points) and Leucaena leucocephala (green points).
Species codes: Ladybirds: CHESUL: Cheilomenes sulphurea; CHIINF: Chilocorus infernalis; CHINIG: Chilocorus nigritus; COCSEP: Coccinella septempunctata; DYSBIS: Dysis bisquatuorguttata; EXOLAE: Exochomus laeviusculus; NEPOBL: Nephus oblongosignatus; NEPVOE: Nephus voeltzkowi; OLANIG: Olla v-nigrum; PARINC: Parastethorus incompletus; PLACAP: Platynaspis capicola; PSEPAL: Pseudoscymnus pallidicollis; PSYVAR: Psyllobora variegata; RHYLOP: Rhyzobius lophanthae; NOVFUM: Novius fumidus; SCYCON: Scymnus constrictus; See Table 1 for site codes.
The first canonical analysis including all data was statistically significant (F-value = 2.71, Df = 7, P-value = 0.001) and explained 50.02% of the total variance. The conditioned variables linked to the site (i.e., Simpson’s Landscape Diversity Index, fragmentation and psyllid_host_plant_cover) explained 37.35% of the total variance, while the explanatory variables (i.e., monthly average_temperature, cumulated rainfall and solar intensity_radiation and prey_abundance) explained 12.07% of the total variance. In the general model, the monthly average temperature and the psyllid host plant cover significantly influence the structure of the entire psyllophagous ladybird community (F-value = 5.51, Df = 1, P-value = 0.001; F-value = 5.05, Df = 1, P-value = 0.004, respectively).
Ladybird community structure in specific-host-plant
Leucaena leucocephala - We found eleven ladybird species associated with Leucaena leucocephala, with a total of 3,621 adults and 1,447 juveniles. The site ESL and MAK were the most diverse, with 8 and 6 species collected, respectively. The site ESP had the greatest abundance of ladybirds, with an average of 19.21 adults and 2.32 juveniles per tree in average, ahead of MAK, with an average of 14.64 adults and 7.42 juveniles per tree in average. The two most abundant species were Exochomus laeviusculus and Olla v-nigrum, with 2,915 and 600 individuals, respectively, i.e., 80.5% and 16.6% of the total individuals collected at all low elevation sites (Fig 2). Canonical analysis conducted on the ladybird community associated with L. leucocephala (cf second RDA model in section statistical analysis) is not statistically significant (F-value = 1.01, Df = 4, P-value = 0.422), and no variables emerge as a significant driver of ladybird’s abundance matrix.
Acacia heterophylla - We found eleven ladybird species associated with Acacia heterophylla, with a total of 638 adults and 92 juveniles. The sites TH and MAIB showed the highest richness, with six species recorded at each site (Fig. 2). In addition, VOLH exhibited the highest relative abundance of ladybirds per tree, with an average of 4.91 adults and 0.14 juveniles per tree, followed by MAIB, with 2.11 adults and 0.22 juveniles per tree. However, in terms of total abundance, Coccinella septempunctata was the most abundant species across all sites, with 415 adults and 45 juveniles collected. Canonical analysis conducted on the ladybird community associated with Acacia heterophylla is not statistically significant (F-value = 0.76, Df = 4, P-value = 0.70, and no variables emerge as a significant driver of the ladybird’s abundance matrix variance.
Presence and abundance of species whose life cycle depends on psyllid
Leucaena leucocephala - Models show (Table 2A) that the presence of E. laeviusculus adults was negatively influenced by landscape fragmentation and by host plant cover and positively influenced by Simpson’s Landscape Diversity Index and prey abundance. The presence of O. v-nigrum adults and juveniles (Table 2A & B) was only influenced by prey abundance.
The abundance of E. laeviusculus adults (Table 3A) was negatively influenced by landscape fragmentation and by host plant cover, and positively influenced by landscape diversity and prey abundance, but not by climate. Abundance of E. laeviusculus juveniles (Table 3B) was only positively influenced by prey abundance. Abundance of O. v-nigrum adults and juvenils (Table 3A & B) was not influenced by parameters included in our models.
Acacia heterophylla - The low number of Coccinella septempunctata juveniles collected during our sampling did not allow us to test the influence of all the landscape-related parameters on their abundance and the presence/absence model did not converge. Thus, we performed the analysis on adults alone (Table 2A).
The presence of Coccinella septempunctata adults (Table 2A) was positively influenced by host plant cover and prey abundance. The effect of the weather (rainfall) on the abundance of C. septempunctata adults (Table 3A) was near to the significance threshold. For C. septempunctata juveniles (Table 3B), temperature had a significant positive effect on their abundance.
Discussion
Species richness
We identified 16 species of ladybirds associated with the psyllid resource, 15 species were found at the adult stage and 6 at the juvenile stage. Poussereau et al. 2018 described 26 ladybird species in Reunion island. This species richness increased after reports of Coccinella septempunctata in 2020 [82] and the description of Nephus apolonia by Magro et al. 2020. The species richness identified around psyllid resources represented about 55% of the total ladybird diversity on the island.
Only 3 of the 16 species were collected in large quantities (over 20 individuals). Thus, our community of psyllophagous ladybirds was mainly composed of rare species, with three predominant species. This follows a classic pattern found in community ecology [83], which also applies to ladybirds [27,84].
Six of these species are natives to Reunion island: Scymnus constrictus Mulsant, 1850, Cheilomenes sulphurea (Olivier, 1791), E. laeviusculus, Dysis bisquatuorguttata Mulsant, 1850, Platynaspis capicola Crotch, 1874 and Psyllobora variegata (Fabricius, 1781). Other species were either introduced accidentally or, in most cases, deliberately for biological control programmes. Only C. septempunctata is native to temperate climates. Among the 15 adult species, four are mentioned as psyllophagous in the literature, namely E. laeviusculus, D. bisquatuorguttata, P. capicola, and O. v-nigrum [70–72]. While E. laeviusculus and O. v-nigrum were the most abundant species in our study, the rarity of D. bisquatuorguttata and P. capicola can be attributed to different factors. Chazeau (1974) [70] described D. bisquatuorguttata as an infrequent species reflecting its naturally low abundance. P. capicola, despite its noted tolerance to climatic variability [70], may face competition from the numerous exotic ladybird species that dominate the island’s ecosystems [85]. Investigating whether specific site characteristics, such as landscape [33] or prey availability, provide a competitive advantage to native species like P. capicola would be an interesting avenue for future research. It is likely that the other species are present because they feed on psyllids, which are accepted or alternative prey (e.g., Chilocorus nigritus (Fabricius, 1798) and Novius fumidus (Mulsant, 1850)). Other species may use the resources associated with psyllids or the host plant (sooty mould, honeydew, e.g., P. variegata) [28].
Lastly, six species were collected in the juvenile stage, which suggests that they complete their life cycle on psyllids, using this resource as an essential prey. Among them, one larva of C. nigritus, one of N. fumidus, both strictly coccidiphagous, and one larva of P. variegatea, strictly mycophagous, are clearly accidentale collections [71]. The other three species, E. laeviusculus, O. v-nigrum, and C. septempunctata, were found in sufficient abundance to rule out the hypothesis of accidental collections. The detection of predatory ladybird larvae alongside a specific prey species is typically viewed as reliable evidence for assessing prey specificity in a natural setting. However, caution is advised in habitats with multiple potential prey species.
E. laeviusculus is a generalist species that feeds on aphids, mealybugs or psyllids as essential prey. This species is relatively small, with an average size of 3.6 mm [72]. It is the smallest species relying on psyllids for its life cycle in our study. Olla v-nigrum is described in the literature as a specialist predator that eats aphids and psyllids [15]. This tropical ladybird is native to French Polynesia and was voluntarily introduced to Reunion island in 1990 as part of a biological programme to control the psyllid H. cubana [63]. Olla v-nigrum measures between 4.4 and 6.0mm [86], which makes it the medium-sized species whose life cycle depends on psyllids in our study.
Contrary to E. laeviusculus and O. v-nigrum, C. septempunctata is widely known as a continental aphidophagous species [87–89]. Originally from Eurasia, a temperate continental region, its presence in Reunion island was reported in March 2020. This species measures between 5.0 and 8.0 mm [90] and is the largest species whose life cycle depends on psyllids in our study. The climate in Reunion island is almost temperate at high elevations, therefore, it is not surprising that C. septempunctata is found at high elevations. However, given its food preference, its presence in adult and larval stages on the psyllid A. uncatoides populations was unexpected. Their unusual use of psyllids as essential prey could be explained by the lifting of dormancy, which may occur in Reunion island in October, with the increase in daylight hours and temperature [91]. It is possible that C. septempunctata is abundant on aphids at high elevations and some individuals make a host jump.C. septempunctata populations are often observed in psylla colonies on both wild and cultivated pistachio trees in the spring and autumn, which coincides with the periods when there is a decline in the aphid populations found on herbaceous plants [92,93]. Mills [94] also noted in 1981 that during the early and late seasons, adults may be observed in association with prey types and habitats not used for reproduction. Furthermore, the anatomy of C. septempunctata is not adapted to the shrub layer because it lacks an enlarged anal disc that would help prevent it from falling [95]. In its native habitat, C. septempunctata prefers herbaceous to shrubby strata [96]. This species is rarely found on trees, such as A. heterophylla. We only found C. septempunctata juveniles at volcanic sites (VOLH and VOLB), where A. heterophylla are smaller.
Community structuration
We were able to demonstrate that the psyllophagous ladybird community was structured by the psyllid host plant and the monthly average temperature in a tropical island environment. We found 11 species associated with A. heterophylla and 11 with L. leucocephala. It was also far less abundant than the low elevation community, associated with L. leucocephala (730 individuals associated with A. heterophylla versus 5068 with L. leucocephala). The results are not surprising given the differences between the two sub-communities in terms of landscape, climate, host plants and psyllid species. The lack of predators at high elevations means that psyllid populations are not controlled [97,98], and annual outbreaks occur [65]. The area of distribution of the psyllid host plant Leucaena leucocephala extends from 0 to 400 m above sea level and that of Acacia heterophylla from an elevation of 1400 to 2000 m (Strasberg et al. 2005; Le Roux et al. 2014). Therefore, the two variables, psyllid host plant and monthly average temperature, are correlated. Moreover, psyllid species are strongly associated with plant species (A. uncatoides on A. heterophylla and H. cubana on L. leucocephala). We cannot clearly determine which of the three variables – monthly average temperature, psyllid host plant or psyllid species - has the most influence on ladybird community structure.
When studied separately, none of the studied factors related to landscape, climate or prey resources structure the two sub-communities. Camarota et al. [99] have shown that landscape structure has no significant influence on the distribution of insect species in tropical forests. However, it is widely demonstrated that landscape composition [7,33,38,100], climate [101,102], and prey availability are the primary factors that induce ladybird assemblages; adults seek prey not only for their own welfare, but as a resource for their progeny [24–27,29,100]. It is possible that in our tropical environment, the psyllid resource is not essential for ladybird communities because a large number of ladybird species feed on psyllids as an alternative or accepted prey. The non-significant result may also indicate that the variables considered in our analysis, which were selected on the basis of knowledge or hypotheses, may not be the main drivers of the community patterns observed. It would be interesting to study other factors that influence ladybird communities, for example, other psyllid species [103], agrochemical use [104–106], the invasion rate of non-native species [100,107–110], or interactions with other predators or parasites [111–116]. The temporal scale should also be considered [117] to improve our understanding of the fluctuations in the ladybird communities
Species whose life cycle depends on psyllid
We demonstrate that the main area of distribution of the two tropical species, whose life cycle depends on the psyllids, Exochomus laeviusculus and Olla v-nigrum, is at lower elevations. The temperate species collected, Coccinella septempunctata, was only found at higher elevations with a more temperate climate.
We showed that psyllid abundance had a positive influence on the presence of all psyllophagous ladybird species, both adults and juveniles. Adults are mobile organisms that can disperse between different environments. Prey attracts and constitutes a stopping point for dispersing adults. Ladybirds lay their eggs in sites where they feed. Therefore, the factors that influence the distribution of larvae are likely to be similar to those affecting adult distribution [101,118]. Egg laying follows successful predation. Various factors influence the number of eggs laid and the duration of egg laying. For example, Honek (1980) identified that C. septempunctata starts laying when the aphid population reaches approximately one aphid per 300 cm² of leaf surface, a threshold that is consistent across different crops. Hemptinne and Dixon 1991 [32] reported that A. bipunctata, which prefers clusters of aphids, starts ovipositing at a higher minimum density of about two aphids per 150 cm². In our case, adult psyllophagous ladybirds lay eggs on essential resources, which means the abundance of psyllids directly influences the presence of larvae.
Psyllid abundance positively influences the abundance of E. laeviusculus adults and juveniles, but not the other species. Due to its smaller size, E. laeviusculus can target psyllids at different stages of their development, often feeding on their small larvae or eggs. This has not been observed in larger species [119]. Compared to larger ladybirds, small aphid-eating ladybirds thrive even when aphid numbers are low. Smaller ladybirds may feed on colonies of aphids early in the aphid population increase, while larger species arrive later [31]. This can explain why E. laeviusculus responds better to psyllid density. Unlike generalist ladybirds, such as E. laeviusculus, specialist species, such as O. v-nigrum, only perform well on a few types of prey. This is a further demonstration that specialist ladybirds can persist at lower aphid densities than generalists [119,120]. In temperate continental environments, habitat generalists may have an advantage over specialists because, despite being less competitive, they can tolerate a wider range of environmental conditions [121,122]. Exotic species, including ladybirds, are also widely recognized as being more successful colonizers than native species [8,123], both in temperate continental [35,85] and insular [124] environments. In tropical island environments, ecological release often disfavors larger species, as competition with native species and resource limitations can hinder their establishment, as observed with Harmonia axyridis in the Azores [125]. This dynamic may benefit smaller species, allowing them to thrive in environments with fewer predators and abundant resources, thereby conserving energy [126]. Therefore, Exochomus laeviusculus has several natural advantages, namely, a generalist diet and a smaller size. In comparison, Olla v-nigrum, another island species, appears to be less competitive due to its own ecological release, despite being larger and more specialized.
Our results show that the landscape influenced the presence and abundance of adults of tropical and temperate psyllophagous ladybird species in a tropical island environment. Several authors have reported the influence of landscape diversity and fragmentation on insect communities [102,127,128], including ladybird species [33,129,130]. Lange et al. 2023 [128] also highlight that plant diversity encourages the establishment of natural grassland communities and stabilizes insect assemblages.
In addition, our results show that the landscape does not have the same influence on the three species that depend on psyllids. The presence and abundance of the generalist E. laeviusculus (both adults and juveniles) are influenced by the landscape at all levels (diversity, fragmentation and host plant covering). This is not the case for C. septempunctata and O. v-nigrum. Statistically, a more diverse landscape is favourable to generalist species because it offers a greater variety of prey [131,132], despite lower local abundance [133–135]. Landscape fragmentation hinders ladybird movement because in a fragmented landscape, encountering an unfavourable habitat is more likely [136]. The small size of E. laeviusculus may reduce its flying ability compared to O. v-nigrum and C. septempunctata [34]. The comparative size of the coccinellid and its prey is also a determining factor when it comes to feeding preference. An analysis of ladybirds’ prey indicates that the smaller the ladybird species, the smaller the prey and/or the greater the ladybird’s mobility [137]. This may explain why E. laeviusculus is more sensitive to landscape fragmentation than other species. More specialized ladybirds, such as O. v-nigrum, are less mobile because they can tolerate low prey densities [119], which means they are less influenced by the landscape. Lastly, according to the “predator satiation hypothesis” defined by Sweeney and Vannote [138] in 1982, an increase in host plant cover, correlated with prey availability at the landscape scale, dilutes E. laeviusculus populations.
Conclusion
In conclusion, this study on ladybird species that interact with psyllid populations in Reunion island reveals unexpected species richness. We observed a mix of rare and predominant ladybird species, with a few common species. The community structure can be explained by the prey species associated with climatic parameters, such as monthly average temperature. It highlights the diversity and ecology of ladybird species, emphasizing the importance of both native and introduced species in the ecosystem. In the tropical island environment of Reunion Island, the findings underscore the influence of environmental factors like elevation, temperature and landscape on the ladybird species depending on their origin and life traits. This study highlights the unbalanced ratio between Hemiptera pests and predators, such as ladybirds, particularly at high elevations. More generally, the study helps improve our understanding of the role that ladybirds play in biological control [139] and ecosystem balance [140], offering insights for future conservation and management strategies in tropical environments.
Supporting information
S1 Table. Summary of landscape metrics for sampling sites, including site identification, fragmentation (number of patches), host plant covering (in square meters), and Simpson’s diversity index for landscape composition.
https://doi.org/10.1371/journal.pone.0320898.s001
(DOCX)
S2 Fig. Spatial maps of sampling sites showing land-use categories within a 1-km radius, used for calculating landscape metrics such as fragmentation, host plant covering, and Simpson’s diversity index.
https://doi.org/10.1371/journal.pone.0320898.s002
(DOCX)
Acknowledgments
We thank The Parc National de La Réunion, The Office National des Forêts and the Conservatoire du Littoral for authorising the sampling on their sites. We would like to thank Samuel Nibouche for proofreading the manuscript.
We wish to express our thanks to all students, David Idmont, Thomas Nacaouelle, Manon Dijoux, Coline Dubois, Pauline de Martin de Viviés, Théo Sechet, Evan Techer, Saïna El Had et Luna Kim-Foo, who helped with the fieldwork, sample sorting and data encoding.
References
- 1. Vellend M. Conceptual synthesis in community ecology. Q Rev Biol. 2010;85(2):183–206.
- 2. Anderson TM, Ritchie ME, McNaughton SJ. Rainfall and soils modify plant community response to grazing in Serengeti National Park. Ecology. 2007;88(5):1191–201.
- 3. Boukoftane A, Benrima A. Effect of climatic factors on spatiotemporal distribution of aphids of citrus fruits in central Mitidja (Algeria). Agro B. 2018;8(1):958–66.
- 4. Corcos D, Cerretti P, Mei M, Vigna Taglianti A, Paniccia D, Santoiemma G, et al. Predator and parasitoid insects along elevational gradients: role of temperature and habitat diversity. Oecologia. 1 setembre 2018;188(1):193–202.
- 5. Facey SL, Ellsworth DS, Staley JT, Wright DJ, Johnson SN. Upsetting the order: How climate and atmospheric change affects herbivore-enemy interactions. Curr Opin Insect Sci. 2014;5:66–74. pmid:32846744
- 6. Srivastava DS, Céréghino R, Trzcinski MK, MacDonald AAM, Marino NAC, Mercado DA, et al. Ecological response to altered rainfall differs across the Neotropics. Ecology. 2020;101(4):e02984. pmid:31958151
- 7. Egerer MH, Bichier P, Philpott SM. Landscape and local habitat correlates of lady beetle abundance and species richness in urban agriculture. Ann Entomol Soc Am. 2017;110(1):97.
- 8.
Tilman D. Mechanisms of plant competition for nutrients: The elements of a predictive theory of competition. 1990;117–41.
- 9.
Tilman D. Resource competition and community structure. Princeton University Press; 1982:308.
- 10. Stevens RD, Willig MR. Geographical ecology at the community level: Perspectives on the diversity of New World bats. Ecology. 2002;83(2):545–60.
- 11. Simberloff D, Dayan T. The guild concept and the structure of ecological communities. Annu Rev Ecol Syst. 1991;22(1):115–43.
- 12. Snyder WE. Coccinellids in diverse communities: Which niche fits?. Biological Control. 2009;51(2):323–35.
- 13. Ślipiński A, Tomaszewska W. Coccinellidae Latreille, 1802. Coccinellidae Latreille, 1802. 2011;454–72.
- 14. Bouchard P, Smith ABT, Douglas H, Gimmel ML, Brunke AJ, Kanda K. Biodiversity of coleoptera. Insect Biodivers. 2017;337–417.
- 15. Hodek I, Honěk A. Scale insects, mealybugs, whiteflies and psyllids (Hemiptera, Sternorrhyncha) as prey of ladybirds. Biol Control. 2009;51(2):232–43.
- 16. Obrycki JJ, Harwood JD, Kring TJ, O’Neil RJ. Aphidophagy by coccinellidae: Application of biological control in agroecosystems. Biol Control. 2009;51(2):244–54.
- 17. Sutherland AM, Parrella MP. Mycophagy in coccinellidae: Review and synthesis. Biol Control. 2009;51(2):284–93.
- 18. Polis GA, Holt RD. Intraguild predation: The dynamics of complex trophic interactions. Trends Ecol Evol. 1 maig 1992;7(5):151–4.
- 19. Alyokhin A, Sewell G. Changes in a lady beetle community following the establishment of three alien species. Biol Invasions. 2004;6(4):463–71.
- 20. Bahlai CA, Colunga-Garcia M, Gage SH, Landis DA. Long-term functional dynamics of an aphidophagous coccinellid community remain unchanged despite repeated invasions. PLOS ONE. 2013;8(12):1–11.
- 21. Bahlai CA, Colunga-Garcia M, Gage SH, Landis DA. The role of exotic ladybeetles in the decline of native ladybeetle populations: Evidence from long-term monitoring. Biol Invasions. 2015;17(4):1005–24.
- 22. Kenis M, Adriaens T, Brown PMJ, Katsanis A, Martin G, Branquart E. Assessing the ecological risk posed by a recently established invasive alien predator: Harmonia axyridis as a case study. BioControl. 2017;62(3):341–54.
- 23. Grez AA, Zaviezo T, Casanoves F, Oberti R, Pliscoff P. The positive association between natural vegetation, native coccinellids and functional diversity of aphidophagous coccinellid communities in alfalfa. Insect Conserv Divers. 2021;14(4):464–75.
- 24. Galecka B. The influence of patches of wood in fields on changes in the numbers of potato aphids and predatory Coccinellidae. Ekol Pol. 1962;10(2):21–44.
- 25. Neuenschwander P, Hagen KS, Smith RF. Predation on aphids in California’s alfalfa fields. Hilgardia. 1975;43:53–78.
- 26. Radcliffe EB, Weires RW, Stucker RE, Barnes DK. Influence of cultivars and pesticides on pea aphid, spotted alfalfa aphid, and associated arthropod taxa in a Minnesota alfalfa ecosystem. Environ Entomol. 1976;5(6):1195–207.
- 27. Honěk A. Distribution and habitats. Ecology Behav Coccinellidae. 2012;110–40.
- 28.
Hodek I. Food relationships. En: Ecology of coccinellidae [Internet]. Dordrecht: Springer Netherlands; 1996;143–238. Disponible a: http://link.springer.com/10.1007/978-94-017-1349-8_6
- 29. Agarwala BK, Bardhanroy P. Numerical response of ladybird beetles (Col., Coccinellidae) to aphid prey (Hom., Aphididae) in a field bean in north‐east India. J Applied Entomology. 1999;123(7):401–5.
- 30. Evans EW. Searching and reproductive behaviour of female aphidophagous ladybirds (Coleoptera: Coccinellidae): A review. Eur J Entomol. 2003;100(1):1–10.
- 31. Honěk A, Dixon AFG, Martinková Z. Body size and the temporal sequence in the reproductive activity of two species of aphidophagous coccinellids exploiting the same resource. Eur J Entomol. 2008;105(3):421–5.
- 32. Hemptinne JL, Dixon A. Why ladybirds have generally been so ineffective in biological control? Behav Impact Aphidophaga. 1991:149–57.
- 33. Gardiner MM, Landis DA, Gratton C, Schmidt N, O’Neal M, Mueller E, et al. Landscape composition influences patterns of native and exotic lady beetle abundance. Diversity Distrib. 2009;15(4):554–64.
- 34. Hemptinne JL, Magro A, Evans EW, Dixon AFG. Body size and the rate of spread of invasive ladybird beetles in North America. Biol Invasions. 2011;14(3):595–605.
- 35. Soares AO, Honěk A, Martinkova Z, Brown PMJ, Borges I. Can native geographical range, dispersal ability and development rates predict the successful establishment of alien ladybird (Coleoptera: Coccinellidae) species in Europe?. Front Ecol Evol. 2018;6:57.
- 36. Honek A, Martinkova Z, Kindlmann P, Ameixa OMCC, Dixon AFG. Long‐term trends in the composition of aphidophagous coccinellid communities in Central Europe. Insect Conserv Diversity. 2013;7(1):55–63.
- 37. Honek A, Dixon AF, Soares AO, Skuhrovec J, Martinkova Z. Spatial and temporal changes in the abundance and composition of ladybird (Coleoptera: Coccinellidae) communities. Curr Opin Insect Sci. 2017;20(1):61–7.
- 38. Yang L, Zeng Y, Xu L, Liu B, Zhang Q, Lu Y. Change in ladybeetle abundance and biological control of wheat aphids over time in agricultural landscape. Agr Ecosyst Environ. 2018;255:102–10.
- 39.. José Adriano Giorgi, Natalia J. Vandenberg, Joseph V. McHugh, Juanita A. Forrester, S. Adam Ślipiński, Kelly B. Miller, et al. The evolution of food preferences in Coccinellidae. Biological Control. 2009;51(2): 215–231. https://doi.org/10.1016/j.biocontrol.2009.05.019
- 40. Mensah RK, Madden JL. Life history and biology of Ctenarytaina thysanura Ferris and Klyver (hemiptera: Psyllidae) on Boronia megastigmanees Ex Bartl. (Rutaceae) in Tasmania. Aust J Entomol. 1993;32(4):327–37.
- 41. Michaud JP. Numerical response of Olla v-nigrum (Coleoptera: Coccinellidae) to infestations of Asian citrus psyllid (Hemiptera: Psyllidae) in Florida. Fl Entomol. 2001;84(4):608–12.
- 42. Michaud JP, Olsen LE. Suitability of asian citrus psyllid, Diaphorina citri, as prey for ladybeetles. BioControl. 2004;49(4):417–31.
- 43. Pluke RWH, Escribano A, Michaud JP, Stansly PA. Potential impact of lady beetles on Diaphorina citri (Homoptera: Psyllidae) in Puerto Rico. flen. Fl Entomol. Juny 2005;88(2):123–8.
- 44. Knowlton GE. Ladybird beetles as predators of the potato psyllid. Can Entomol. 1933;65(11):241–3.
- 45. Leeper J, Beardsley JW. The biological control of Psylla uncatoides (Ferris & Klyver) (Homoptera: Psyllidae) on Hawaii. Proc Hawaiian Entomol Soc. 1976;22(2):307–21.
- 46. Nakahara L, Nagamine W, Matayoshi S, Kumashiro B. Biological control program of the Leucaena psyllid, Heteropsylla cubana Crawford (Homoptera: Psyllidae) in Hawaii. Leucaena Res Rep. 1987;7(2):39–44.
- 47. Diraviam J, Viraktamath CA. Population dynamics of the introduced ladybird beetle, Curinus coeruleus Mulsant in relation to its psyllid prey Heteropsylla cubana Crawford in Bangalore. J Biol Control. 1990;4(2):99–104.
- 48. Vandeschricke F, Quilici S, Gauvin J, Roederer Y. Le psylle du Leucaena à la Réunion. Importance des dégâts et perspectives de lutte biologique. Bois For Trop. 1992;234(47):47–59.
- 49. Askari seyahooei M, Sadeghi A, Samavi S. Study on the possibility of biological control of citrus Asian psyllid, Diaphorina citri, in Iran. ISAST. 2012;1–17.
- 50. Pugh AR, O’Connell DM, Wratten SD. Further evaluation of the southern ladybird (Cleobora mellyi) as a biological control agent of the invasive tomato–potato psyllid (Bactericera cockerelli). Biol Control. 2015;90:157–63.
- 51. Khan AA, Qureshi JA, Afzal M, Stansly PA. Two-spotted ladybeetle adalia bipunctata L. (Coleoptera: Coccinellidae): A commercially available predator to control asian citrus psyllid diaphorina citri (Hemiptera: Liviidae). PLoS One. 2016;11(9):e0162843. pmid:27631730
- 52. Pérez-González O, Tamez-Guerra P, Flores AAO, Aguirre-Arzola VE. Curinus coeruleus as potential natural enemy of Diaphorina citri in citrus orchards at Nuevo Leon, Mexico. swen. 2022.;47(2):519–22.
- 53. Özgen İ, Mamay M, Yanık E. Release of the lady beetle (Oenopia conglobata L.) to control the common pistachio psylla. Biol Control. 2022;171:104940.
- 54. Burckhardt D. Psylloid pests of temperate and subtropical crop and ornamental plants (Hemiptera, Psylloidea): A review. Trends Agric Sci Entomol. 1994;2:173–86.
- 55. Munyaneza JE. Psyllids as vectors of emerging bacterial diseases of annual crops. swen. 2010;35(3):471–7.
- 56. Cen Y, Yang C, Holford P, Beattie GAG, Spooner-Hart R, Liang G, et al. Feeding behaviour of the Asiatic citrus psyllid, Diaphorina citri, on healthy and huanglongbing-infected citrus. Entomol Exp Appl. 2012;143(1):13–22.
- 57. Ameline A, Karkach A, Denoirjean T, Grondin M, Molinari F, Turpin P, et al. Bacterial plant pathogens affect the locomotor behavior of the insect vector: a case study of Citrus volkameriana–Triozae erytreae–Candidatus Liberibacter asiaticus system. Insect Sci. 2023;0:1–10.
- 58. Capoor SP, Rao DG, Viswanath SM. Diaphorina citri Kuway., A vector of the greening disease of Citrus in India. Indian J Agric Sci. 1967;37(6):572–6.
- 59. Reynaud B, Turpin P, Molinari FM, Grondin M, Roque S, Chiroleu F, et al. The African citrus psyllid Trioza erytreae: An efficient vector of Candidatus Liberibacter asiaticus. Front Plant Sci. 2022;13.
- 60. Aléné DC, Djiéto-Lordon C, Tadu Z, Burckhardt D. Infestation of Heteropsylla cubana (Hemiptera: Psylloidea) on Leucaena leucocephala (Fabaceae: Mimosoideae) in Cameroon. Afr Entomol. 2012;20(2):207–16.
- 61. Bastin S, González Hernández H, Siverio F, Ouvrard D, Hernández Suárez E. Primera cita de Heteropsylla cubana Crawford, 1914 (Hemiptera, Psyllidae) para las Islas Canarias y España. Bol Soc Entomol Arag. 2021;68:437–8.
- 62. Beardsley JW, Uchida GK. Parasites associated with the Leucaena psyllid, Heteropsylla cubana Crawford, in Hawaii. J Hawaii Inst Trop Agric Hum Res. 1990;30(3411):155–6.
- 63. Quilici S, Francki A, Montagneux B, Tassin J. Successful establishment on Reunion Island of an exotic ladybird, Olla v-nigrum the biocontrol of leucaena psyllid, Heteropsylla cubana. Actes Atelier Psyllide Leucaena. 1995. https://agritrop.cirad.fr/389886/
- 64.
Chazeau J, Bouye E, Larbogne de L. Development and life table of Olla v-nigrum (Col.: Coccinellidae), a natural enemy of Heteropsylla cubana (Hom.: Psyllidae) introduced in New Caledonia. 1991
- 65.
Angebault G, Vinot M, Marquereau L, Dervin S, Salamolard M, Rouget M, et al. Population dynamics and damages of the invasive phloem-feeder psyllid Acizzia uncatoides (Hemiptera: Psyllidae) on the endemic tree Acacia heterophylla on La Reunion Island. 2019;80.
- 66. Strasberg D, Rouget M, Richardson DM, Baret S, Dupont J, Cowling RM. An assessment of habitat diversity and transformation on La Réunion island (Mascarene islands, indian ocean) as a basis for identifying broad-scale conservation priorities. Biodivers Conserv. 2005;14(12):3015–32.
- 67. Le Roux JJ, Strasberg D, Rouget M, Morden CW, Koordom M, Richardson DM. Relatedness defies biogeography: the tale of two island endemics (A cacia heterophylla and A. koa). New Phytol. octubre 2014;204(1):230–42.
- 68. Badosa J, Haeffelin M, Kalecinski N, Bonnardot F, Jumaux G. Reliability of day-ahead solar irradiance forecasts on Reunion Island depending on synoptic wind and humidity conditions. Sol Energy. 2015;115:306–21.
- 69. Institut national de l’information géographique et forestière (IGN). RGE ALTI® [Internet]. 2023. Disponible a: https://geoservices.ign.fr/rgealti.
- 70. Chazeau J, Etienne J, Fursh H. Les Coccinellidae de l’ile de La Reunion (Insecta Coleoptera). Bull Mus Natl Hist Nat. 1974;210(1):265–97.
- 71.
Quilici S, Vincenot D, Franck A. Les auxiliaires des cultures fruitières à l’île de la Réunion. Editions Quae. 2003;180.
- 72.
Poussereau J, Coutanceau J, Nicolas V, Gomy Y. Les coccinelles de la Réunion. Orphie. 2018;98.
- 73. Magro A, Churata-Salcedo J, Lecompte E, Hemptinne J, Almeida L. A new species of Nephus (Nephus) (Coleoptera, Coccinellidae) described from Reunion Island. ZooKeys. 2020;962:123.
- 74. Huang W, Xie X, Huo L, Liang X, Wang X, Chen X. An integrative DNA barcoding framework of ladybird beetles (Coleoptera: Coccinellidae). Sci Rep. 2020;10(1):10063.
- 75.
Le Mezo L, Dupuy S, Gaetano R. La Réunion - occupation du sol - carte 2022 (Spot6/7) - 1.5m. 2022. https://doi.org/10.18167/DVN1/F0SUQC
- 76. Legendre P, Gallagher ED. Ecologically meaningful transformations for ordination of species data. Oecologia. 2001;129(2):271–80.
- 77. Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. vegan: Community ecology package. 2022. https://cran.r-project.org/web/packages/vegan/index.html
- 78. Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015;67(1):1–48.
- 79. Van De Pol M, Wright J. A simple method for distinguishing within- versus between-subject effects using mixed models. Anim Behav. 2009;77(3):753–8.
- 80. Hurlbert S. Pseudoreplication and the design of ecological field experiments. Ecol Monogr. 1984;54(2):187–211. https://esajournals.onlinelibrary.wiley.com/doi/abs/10.2307/1942661
- 81. Zuur AF, Leno EN, Walker N, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R. 2009. https://link.springer.com/book/10.1007/978-0-387-87458-6
- 82.
Préfet de La Réunion. Communiqué de presse: Détection d’une espèce de Coccinelle exotique à la Réunion. 2020.
- 83.
Krebs CJ. Ecology: The experimental analysis of distribution and abundance. 6. ed. Prson new International ed. Harlow: Pearson. 2014;646.
- 84. Smith BC. Effects of various factors on the local distribution and density of coccinellid adults on corn (Coleoptera: Coccinellidae). Can Entomol. 1971;103(8):1115–20.
- 85. Roy HE, Adriaens T, Isaac NJB, Kenis M, Onkelinx T, Martin GS, et al. Invasive alien predator causes rapid declines of native European ladybirds. Diversity Distrib. 2012;18(7):717–25.
- 86.
Slipinski A, Pang H, Pang H. Ladybird beetles of the Australo-Pacific region: Coleoptera: Coccinellidae: Coccinellini. 2019;240.
- 87. Angalet GW, Tropp JM, Eggert AN. Coccinella septempunctata in the United States: Recolonizations and notes on its ecology. Environ Entomol. 1979;8(5):896–901.
- 88. Cartwright BO, Eikenbary RD, Angalet GW, Campbell RK. Release and establishment of Coccinella septempunctata in Oklahoma. Environ Entomol. 1979;8(5):819–23.
- 89. Schaefer PW, Dysart RJ, Specht HB. North American distribution of Coccinella septempunctata (Coleoptera: Coccinellidae) and its mass appearance in coastal Delaware. Environ Entomol. 1987;16(2):368–73.
- 90. Zhou X, Honek A, Powell W, Carter N. Variations in body length, weight, fat content and survival in Coccinella septempunctata at different hibernation sites. Entomol Exp Appl. 1995;75(2):99–107.
- 91. Wang S, Tan XL, Guo XJ, Zhang F. Effect of temperature and photoperiod on the development, reproduction, and predation of the predatory ladybird Cheilomenes sexmaculata (Coleoptera: Coccinellidae). J Econ Entomol. 2013;106(6):2621–9.
- 92.
Jalali MA. Study of food consumption in lady beetles of the common pistachio psyllid, Agonoscena pistaciae in Rafsanjan and compiling a life table in controlled conditions. 2001.
- 93.
Mehrnejad M. The pests of pistachio trees in Iran, natural enemies and control. 2014.
- 94. Mills NJ. Essential and alternative foods for some British Coccinellidae (Coleoptera). Entomol Gaz. 1981;32(3):197–202.
- 95. Leather SR, Cooke RCA, Fellowes MDE, Rombe R. Distribution and abundance of ladybirds (Coleoptera: Coccinellidae) in non-crop habitats. Eur J Entomol. 1999;96:23–7.
- 96. Pruszynski S, Lipa JJ. Observations on life cycle and food specialization of Adalia bipunctata (L.) (Coleoptera, Coccinellidae). Prace Nauk Inst Ochr Róslin. 1970;12:99–116.
- 97.
Dixon AFG. Insect predator-prey dynamics: Ladybird beetles and biological control. Cambridge University Press. 2000;272
- 98.
Kindlmann P, Dixon AFG. Insect predator-prey dynamics and the biological control of aphids by ladybirds. 2002;118–28.
- 99. Camarota F, Dáttilo W, da Silva PG, de Castro FS, do Vale Beirão M, Perillo LN, et al. The spatial distribution of insect communities of a mountaintop forest archipelago is not correlated with landscape structure: A multitaxa approach. Insect Conserv Divers. 2023;16(6):790–800.
- 100. Pan H, Liu B, Jaworski CC, Yang L, Liu Y, Desneux N, et al. Effects of aphid density and plant taxa on predatory ladybeetle abundance at field and landscape scales. Insects. 2020;11(10):695. pmid:33066204
- 101. Honěk A. Factors which determine the composition of field communities of adult aphidophagous Coccinellidae (Coleoptera). Z Angew Entomol. 1982;94(1–5):157–68.
- 102. Tscharntke T, Steffan-Dewenter I, Kruess A, Thies C. Characteristics of insect populations on habitat fragments: A mini review. Ecol Res. 2002;17(2):229–39.
- 103. Ouvrard D. Psyl’list. 2015; https://data.nhm.ac.uk/dataset/psyl-list
- 104. Duru M, Therond O, Martin G, Martin-Clouaire R, Magne MA, Justes E, et al. How to implement biodiversity-based agriculture to enhance ecosystem services: A review. Agron Sustain Dev. 2015;35(4):1259–81.
- 105. Kibulei E, Kudra A, Kabota S, Bakengesa J. Diversity of ladybird beetle communities (Coleoptera: Coccinellidae) under different cucurbit farming practices in Morogoro, Tanzania: Influence of management practices on diversity of ladybird beetles. J Curr Opin Crop Sci. 2023;76–88.
- 106. Reddy BT, Giraddi R. Diversity studies on insect communities in organic, conservation and conventional farming systems under rain-fed conditions. J Entomol Zool Stud. 2019;7(3):883–6.
- 107. Simberloff D. Why do introduced species appear to devastate islands more than mainland areas?. Pac Sci. 1995;49(1):87–97.
- 108. Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E. Quantifying threats to imperiled species in the United States. BioScience. 1998;48(8):607–15.
- 109. Kindlmann P, Ameixa OMCC, Dixon AFG. Ecological effects of invasive alien species on native communities, with particular emphasis on the interactions between aphids and ladybirds. BioControl. 2011;56(4):469–76.
- 110. Lenzner B, Latombe G, Capinha C, Bellard C, Courchamp F, Diagne C, et al. What will the future bring for biological invasions on islands? An expert-based assessment. Front Ecol Evol. 2020;8:1–16.
- 111. Hoogendoorn M, Heimpel GE. Indirect interactions between an introduced and a native ladybird beetle species mediated by a shared parasitoid. Biol Control. 2002;25(3):224–30.
- 112. Riddick EW, Cottrell TE, Kidd KA. Natural enemies of the Coccinellidae: Parasites, pathogens, and parasitoids. Biol Control. 2009;51(2):306–12.
- 113. Howe AG, Ravn HP, Jensen AB, Meyling NV. Spatial and taxonomical overlap of fungi on phylloplanes and invasive alien ladybirds with fungal infections in tree crowns of urban green spaces. FEMS Microbiol Ecol. 2016;92(9):fiw143.
- 114. Haelewaters D, Hiller T, Kemp EA, van Wielink PS, Shapiro-Ilan DI, Aime MC, et al. Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi. PeerJ. 2020;8:1–16. pmid:33194385
- 115. Knapp M, Řeřicha M, Haelewaters D, González E. Fungal ectoparasites increase winter mortality of ladybird hosts despite limited effects on their immune system. Proc Biol Sci. 2022;289(1971):20212538. pmid:35317669
- 116. Vinot M, Hervy F, Sadeyen J, Gomard Y, Razafindrakotomamonjy A, Sookar P, et al. Main Eucalyptus pests and their associated parasitoids with a focus on Madagascar and the Mascarene islands. Int J Trop Insect Sci. 2023;43(6):2263–85.
- 117. Tatsumi S, Iritani R, Cadotte MW. Temporal changes in spatial variation: Partitioning the extinction and colonisation components of beta diversity. Ecol Lett. 2021;24(5):1063–72.
- 118. Honek A. Plant density and occurrence of Coccinella septempunctata and Propylaea quatuordecimpunctata (Coleoptera, Coccinellidae) in cereals. Acta Entomol Bohemoslov. 1979;76(5):308–12.
- 119. Sloggett JJ. Weighty matters: Body size, diet and specialization in aphidophagous ladybird beetles (Coleoptera: Coccinellidae). Eur J Entomol. 2008;105(3):381–9.
- 120. Sloggett JJ, Majerus MEN. Habitat preferences and diet in the predatory Coccinellidae (Coleoptera): An evolutionary perspective. Biol J Linn Soc. 2000;70(1):63–88.
- 121. Marvier M, Kareiva P, Neubert MG. Habitat destruction, fragmentation, and disturbance promote invasion by habitat generalists in a multispecies metapopulation. Risk Anal. 2004;24(4):869–78.
- 122. McIntyre S, Martin TG, Heard KM, Kinloch J. Plant traits predict impact of invading species: An analysis of herbaceous vegetation in the subtropics. Aust J Bot. 2005;53(8):757–70.
- 123. Shea K, Chesson P. Community ecology theory as a framework for biological invasions. Trends Ecol Evol. 2002;17(4):170–6.
- 124. Brown PMJ, Frost R, Doberski J, Sparks T, Harrington R, Roy HE. Decline in native ladybirds in response to the arrival of Harmonia axyridis: Early evidence from England. Ecol Entomol. 2011;36(2):231–40.
- 125. Soares AO, Honěk A, Martinkova Z, Skuhrovec J, Cardoso P, Borges I. Harmonia axyridis failed to establish in the Azores: The role of species richness, intraguild interactions and resource availability. BioControl. 2017;62(3):423–34.
- 126. Clegg SM, Owens PF. The ‘island rule’ in birds: medium body size and its ecological explanation. Proc R Soc B. 2002;269(1498):1359–65.
- 127. Bottero I, Dominik C, Schweiger O, Albrecht M, Attridge E, Brown MJF, et al. Impact of landscape configuration and composition on pollinator communities across different European biogeographic regions. Front Ecol Evol. 2023;11:1–16.
- 128. Lange M, Ebeling A, Voigt W, Weisser W. Restoration of insect communities after land use change is shaped by plant diversity: A case study on carabid beetles (Carabidae). Sci Rep. 2023;13(1):2140.
- 129. Stoner KJL, Joern A. Landscape vs. local habitat scale influences to insect communities from tallgrass prairie remnants. Ecol Appl. 2004;14(5):1306–20.
- 130. Rösch V, Tscharntke T, Scherber C, Batáry P. Landscape composition, connectivity and fragment size drive effects of grassland fragmentation on insect communities. J Appl Ecol. 2013;50(2):387–94.
- 131. Landis DA, Wratten SD, Gurr GM. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol. 2000;45(1):175–201.
- 132. Rusch A, Valantin-Morison M, Sarthou JP, Roger-Estrade J. Biological control of insect pests in agroecosystems: Effects of crop management, farming systems, and seminatural habitats at the landscape scale: A review. Adv Agron. 2010;219–59. https://www.sciencedirect.com/science/article/pii/B9780123850409000062
- 133. Letourneau DK, Armbrecht I, Rivera BS, Lerma JM, Carmona EJ, Daza MC, et al. Does plant diversity benefit agroecosystems? A synthetic review. Ecol Appl. 2011;21(1):9–21. pmid:21516884
- 134. Wan NF, Zheng XR, Fu LW, Kiær LP, Zhang Z, Chaplin-Kramer R, et al. Global synthesis of effects of plant species diversity on trophic groups and interactions. Nat Plants. 2020;6(5):503–10. pmid:32366981
- 135. Barnes AD, Scherber C, Brose U, Borer ET, Ebeling A, Gauzens B, et al. Biodiversity enhances the multitrophic control of arthropod herbivory. Sci Adv. 2020;6(45):eabb6603. pmid:33158860
- 136. With KA, Pavuk DM, Worchuck JL, Oates RK, Fisher JL. Threshold effects of landscape structure on biological control in agroecosystems. Ecol Appl. 2002;12(1):52–65.
- 137. Dixon AFG, Hemptinne JL. Body size distribution in predatory ladybird beetles reflects that of their prey. Ecology. 2001;82(7):1847–56.
- 138. Sweeney BW, Vannote RL. Population synchrony in mayflies: A predator satiation hypothesis. Evolution. 1982;36(4):810–21.
- 139. Michaud JP. Coccinellids in biological control. Ecol Behav Ladybird Beetles. 2012;488–519. https://onlinelibrary.wiley.com/doi/abs/10.1002/9781118223208.ch11
- 140. Soares AO, Haelewaters D, Ameixa OMCC, Borges I, Brown PMJ, Cardoso P, et al. A roadmap for ladybird conservation and recovery. Conserv Biol. 2023;37(1):e13965. pmid:35686511