Mariano Ordano

Understanding Long-Term Fruit Fly (Diptera: Tephritidae) Population Dynamics: Implications for Areawide Management

ABSTRACT Fruit flies (Diptera: Tephritidae) are devastating agricultural pests worldwide but studies on their long-term population dynamics are sparse. Our aim was to determine the mechanisms driving long-term population dynamics as a prerequisite for ecologically based areawide pest management. The population density of three pestiferous Anastrepha species [Anastrepha ludens (Loew), Anastrepha obliqua (Macquart), and Anastrepha serpentina (Wiedemann) ] was determined in grapefruit (Citrus × paradisi Macfad.), mango (Mangifera indica L.), and sapodilla [Manilkara zapota (L.) P. Royen] orchards in central Veracruz, México, on a weekly basis over an 11-yr period. Fly populations exhibited relatively stable dynamics over time. Population dynamics were mainly driven by a direct density-dependent effect and a seasonal feedback process. We discovered direct and delayed influences that were correlated with both local (rainfall and air temperature) and global climatic variation (El Niño Southern Oscillation [ENSO] and North Atlantic Oscillation [NAO]), and detected differences among species and location of orchards with respect to the magnitude and nature (linear or nonlinear) of the observed effects, suggesting that highly mobile pest outbreaks become uncertain in response to significant climatic events at both global and local levels. That both NAO and ENSO affected Anastrepha population dynamics, coupled with the high mobility of Anastrepha adults and the discovery that when measured as rate of population change, local population fluctuations exhibited stable dynamics over time, suggests potential management scenarios for the species studied lie beyond the local scale and should be approached from an areawide perspective. Localized efforts, from individual growers will probably prove ineffective, and nonsustainable.

Inter-specific competition and competition-free space in the tephritid parasitoids Utetes anastrephae and Doryctobracon areolatus (Hymenoptera: Braconidae: Opiinae)

Utetes anastrephae (Viereck) and Doryctobracon areolatus (Szépligeti) are common, native, Neotropical braconid parasitoids of tephritid fruit flies that are sympatric and often found attacking the same host. The coexistence of the two species may be due in part to the longer ovipositor of D. areolatus that permits it to attack larvae in larger fruit than can U. anastrephae. This increases its potential host range and provides ‘competitor‐free space’. The capacity of U. anastrephae to persist in smaller fruit, exploitable by D. areolatus, suggested that it was a superior competitor in multiparasitised hosts. As predicted U. anastrephae had a competitive advantage over D. areolatus and this advantage occurred regardless of the order in which the two parasitoids attacked. Although we could not identify the precise mechanisms used for elimination of competitors, a possible cause is suggested by the formidable mandibles of the first‐instar U. anastrephae. However, D. areolatus survival increased significantly if eggs had been deposited 24 h prior to exposure to U. anastrephae. Older D. areolatus larvae might be more competitive after a period of development. Utetes anastrephae females were less likely to oviposit into hosts previously attacked by D. areolatus than vice versa. This was a second case of the relatively rare phenomenon of inter‐specific discrimination of a previously exploited host within the opiine braconid parasitoids of frugivorous tephritids.

Larval feeding substrate and species significantly influence the effect of a juvenile hormone analog on sexual development/performance in four tropical tephritid flies

The juvenile hormone (JH) analog methoprene reduces the amount of time it takes laboratory-reared Anastrepha suspensa (Caribbean fruit fly) males to reach sexual maturity by almost half. Here, we examined if methoprene exerted a similar effect on four other tropical Anastrepha species (Anastrepha ludens, Anastrepha obliqua, Anastrepha serpentina and Anastrepha striata) reared on natural hosts and exhibiting contrasting life histories. In the case of A. ludens, we worked with two populations that derived from Casimiroa greggii (ancestral host, larvae feed on seeds) and Citrus paradisi (exotic host, larvae feed on pulp). We found that the effects of methoprene, when they occurred, varied according to species and, in the case of A. ludens, according to larval host. For example, in the case of the two A. ludens populations the effect of methoprene on first appearance of male calling behavior and number of copulations was only apparent in flies derived from C. greggii. In contrast, males derived from C. paradisi called and mated almost twice as often and females started to lay eggs almost 1 day earlier than individuals derived from C. greggii, but in this case there was no significant effect of treatment (methoprene) only a significant host effect. There were also significant host and host by treatment interactions with respect to egg clutch size. A. ludens females derived from C. paradisi laid significantly more eggs per clutch and total number of eggs than females derived from C. greggii. With respect to the multiple species comparisons, the treatment effect was consistent for A. ludens, occasional in A. serpentina (e.g., calling by males, clutch size), and not apparent in the cases of A. obliqua and A. striata. Interestingly, with respect to clutch size, in the cases of A. ludens and A. serpentina, the treatment effect followed opposite directions: positive in the case of A. ludens and negative in the case of A. serpentina. We center our discussion on two hypotheses (differential physiology and larval-food), and also interpret our results in light of the life history differences exhibited by the different species we compared.

Olive fruit fly (Bactrocera oleae) population dynamics in the Eastern Mediterranean: Influence of exogenous uncertainty on a monophagous frugivorous Insect

Despite of the economic importance of the olive fly (Bactrocera oleae) and the large amount of biological and ecological studies on the insect, the factors driving its population dynamics (i.e., population persistence and regulation) had not been analytically investigated until the present study. Specifically, our study investigated the autoregressive process of the olive fly populations, and the joint role of intrinsic and extrinsic factors molding the population dynamics of the insect. Accounting for endogenous dynamics and the influences of exogenous factors such as olive grove temperature, the North Atlantic Oscillation and the presence of potential host fruit, we modeled olive fly populations in five locations in the Eastern Mediterranean region. Our models indicate that the rate of population change is mainly shaped by first and higher order non-monotonic, endogenous dynamics (i.e., density-dependent population feedback). The olive grove temperature was the main exogenous driver, while the North Atlantic Oscillation and fruit availability acted as significant exogenous factors in one of the five populations. Seasonal influences were also relevant for three of the populations. In spite of exogenous effects, the rate of population change was fairly stable along time. We propose that a special reproductive mechanism, such as reproductive quiescence, allows populations of monophagous fruit flies such as the olive fly to remain stable. Further, we discuss how weather factors could impinge constraints on the population dynamics at the local level. Particularly, local temperature dynamics could provide forecasting cues for management guidelines. Jointly, our results advocate for establishing monitoring programs and for a major focus of research on the relationship between life history traits and populations dynamics.

A comparison of floral integration between selfing and outcrossing species: a meta-analysis.

BACKGROUND AND AIMS Floral integration is thought to be an adaptation to promote cross-fertilization, and it is often assumed that it increases morphological matching between flowers and pollinators, increasing the efficiency of pollen transfer. However, the evidence for this role of floral integration is limited, and recent studies have suggested a possible positive association between floral integration and selfing. Although a number of explanations exist to account for this inconsistency, to date there has been no attempt to examine the existence of an association between floral integration and mating system. This study hypothesized that if pollinator-mediated pollen movement among plants (outcrossing) is the main factor promoting floral integration, species with a predominantly outcrossing mating system should present higher levels of floral integration than those with a predominantly selfing mating system. METHODS A phylogenetically informed meta-analysis of published data was performed in order to evaluate whether mating system (outcrossing vs. selfing) accounts for the variation in floral integration among 64 species of flowering plants. Morphometric floral information was used to compare intra-floral integration among traits describing sexual organs (androecium and gynoecium) and those corresponding to the perianth (calix and corolla). KEY RESULTS The analysis showed that outcrossing species have lower floral integration than selfing species. This pattern was caused by significantly higher integration of sexual traits than perianth traits, as integration of the latter group remained unchanged across mating categories. CONCLUSIONS The results suggest that the evolution of selfing is associated with concomitant changes in intra-floral integration. Thus, floral integration of sexual traits should be considered as a critical component of the selfing syndrome.

Bird fruit consumption results from the interaction between fruit-handling behaviour and fruit crop size

Bird foraging behaviour is a major factor involved in mutualistic interactions of fleshy-fruited plants. Despite much research, we still lack quantified demonstrations of how fruit display traits affect fruit removal behaviour. Although the fruit crop size hypothesis proposes a general mechanism for fruit trait selection, it overlooks the fact that distinctive bird behaviours in a bird assemblage would have different effects on fruit crop size. Here, we show that the relevance of fruit crop size for bird fruit consumption is driven by two basic components of fruit foraging behaviour: fruit handling and residence time. We assessed bird fruit-eating behaviour (fruit consumption, fruit handling and residence time) and its relationship with fruit crop size, taking into account body size and spatial focal context (conspecific neighbour density and distance to the forest edge from individual plants) in a population of Vassobia breviflora (Solanaceae) in Tucumán, Argentina. At the assemblage level, fruit consumption was positively related to fruit crop size and residence time, and the interaction between fruit crop size and residence time depended on fruit-handling behaviour. At the functional group level, both gulpers and pulp consumers showed a positive relationship between fruit consumption and residence time. However, gulpers showed a negative interaction between fruit crop size and residence time, while pulp consumers showed no interaction. At the species level, fruit consumption by Turdus rufiventris (gulper) was positively related to fruit crop size, whereas fruit consumption by Thraupis sayaca and Zonotrichia capensis (pulp consumers) depended positively on residence time. Essentially, gulpers spent short residence times in plants with larger fruit crops, whereas pulp consumers spent long residence times in plants regardless of fruit crop size. The segregation between fruit-eating behaviours and their relationship with fruit crop size suggests that bird functional groups (i.e. gulpers and pulp consumers) would shape fruit display traits with different intensities.

The role of trait combination in the conspicuousness of fruit display among bird‐dispersed plants

Summary In visually-driven seed dispersal mutualisms, natural selection should promote plant strategies that maximize fruit visibility to dispersers. Plants might increase seed dispersal profitability by increasing conspicuousness of fruit display, understood as a plant strategy to maximize fruit detectability by seed dispersers. The role of different plant traits in fruit choice and consumption by seed dispersers has been broadly studied. However, there is no clear evidence about the importance of the traits that increase conspicuousness of fruit display. Because strategies to maximize conspicuousness of fruit display are diverse, and usually are expected to be costly, we would expect that individual plant species will produce an efficient combination of traits. We explored this prediction with 62 fleshy-fruited plant species of a subtropical Andean forest (Southern Yungas), and using a large dataset of fruit consumption by birds (4,476 records). Conspicuousness of fruit display was characterized by both fruit and plant traits including chromatic contrast, size, exposure, aggregation, and crop size of fruits. We also considered phylogenetic effects on phenotypic variation. Fruit consumption was explained by fruit chromatic contrast depending on fruit crop size. These traits revealed low phylogenetic effects, with the exception of four plant clades at different levels in the phylogenetic tree. Negative correlations between pairs of traits support our assumption that fruit display traits are costly, suggesting natural selection favours parsimonious evolutionary pathways. Plant species seem to rely on conspicuousness of fruit display by a combination of traits that might minimize costs of fruit display. This appears adaptively relevant to improve communication with mutualistic animals, to increase fruit consumption in a community context and, ultimately, to enhance the profitability of seed dispersal. This article is protected by copyright. All rights reserved.

How little is too little?: The adaptive value of floral integration.

For more than a century the idea that natural selection favors high levels of floral integration has prevailed as a paradigm among floral biologists. However, there is very little empirical evidence of the adaptive value of floral integration. In this addendum we highlight an important result derived from an empirical study complemented with a literature review and mathematical simulations. Results indicated that intrafloral integration but not floral integration was selected among four species of Rosaceae. The literature review coupled with null models revealed that flowering plants have on average lower than expected levels of floral integration. Mathematical simulations further demonstrated that observed levels of floral integration might result from selection favoring increased intrafloral integration. Altogether, these findings suggest that in most flowering plants, floral integration has a low adaptive value and could be a by-product of selection favoring intrafloral integration.

Linking the hierarchical decision-making process of fruit choice and the phenotypic selection strength on fruit traits by birds

Aims Animals in search of fleshy fruits forage mostly according to the number of available fruits and then select individual fruits based on reward quality or advertised subtle traits. This hierarchical pattern of fruit choice would be translated into patterns of selection strength mediated by frugivores on fruit display traits. Thus, frugivores would exert higher selection pressures on fruit crop size and lower selection pressures on within-plant variation of phenotypic traits (infructescence, fruit and seed size). However, no attempt to link this behavioral mechanism of hierarchical trait selection to natural selection patterns has been made. Therefore, we sought to determine the relationship between the hierarchical decision-making process of fruit choice and patterns of natural selection on fruit traits. Methods We recorded bird visits and measured fruit-related traits (fruit crop size, fruit diameter and seed weight) in a natural population of Psychotria carthagenensis, a bird-dispersed treelet, in a Yungas forest from Argentina. To assess phenotypic selection patterns on fruit display traits, we performed multivariate selection analysis, and to explicitly identify a hierarchy of fruit trait choice we used a classification tree as a predictive model. Important Findings Selection patterns on fruit display traits were in agreement with a hierarchical process of fruit choice made by birds. The strength of directional selection on the total number of fruits in a plant (i.e. fruit crop size) was nearly two times higher than on fruit size, and the classification tree analysis supported this hierarchical pattern. Our results support previous evidence that seed dispersers shape fruit crop size with higher intensity than subindividual fruit traits. Also, high levels of subindividual phenotypic variation of fruit display traits may be explained by relaxed selection pressures exerted by frugivores. Empirical studies also show that this pattern may constitute a general phenomenon among other plant–animal interactions.

The Strength and Drivers of Bird-Mediated Selection on Fruit Crop Size: A Meta-Analysis

In seed-dispersal mutualisms, the number of fruit a plant displays is a key trait, as it acts as a signal for seed dispersers that entails fruit removal and exportation of reproductive units (fruit crop size hypothesis). Although this hypothesis has gained general acceptance, forces driving the shape and strength of natural selection exerted by birds on fruit crop size remains an unresolved matter. Here, we propose that ecological filters promoting high functional equivalence of interacting partners (similar functional roles) translate into similar selection pressures on fruit crop size, enhancing selection strength on this trait. We performed a meta-analysis on 50 seed-dispersal systems to test the hypothesis that frugivorous birds exert positive selection pressure on fruit crop size, and to assess whether different factors expected to act as filters (fruit diameter, fruit type, fruiting season length, bird functional groups and latitude) influence phenotypic selection regimes on this trait. Birds promote larger fruit crop sizes as a general pattern in nature. Short fruiting seasons and a high proportion of species belonging to the same functional group showed higher selection strength on fruit crop size. Also, selection strength on fruit crop size increased for large-fruited species and towards the tropics. Our results support the hypothesis that fruit crop size represents a conspicuous signal advertising the amount of reward to visually driven interacting partners, and that both plant and bird traits, as well as environmental factors, drive selection strength on fruit display traits. Furthermore, our results suggest that the relationship among forces impinged by phenology and frugivore functional roles may be key to understand their evolutionary stability.