Community ecology of parasites: functional and network approaches

Els organismes i les poblacions en una localitat formen una comunitat biològica. La composició de poblacions en una comunitat pot veure's influenciada per processos estocàstics o deterministes. Generalment aquesta depén del nivell al qual s'estudie la comunitat. Per tal de determinar les regles que regeixen la composició de la comunitat, hem de mesurar característiques descriptives a nivell de comunitat ecològica, com la diversitat de la comunitat. La diversitat és la variabilitat de la vida en una localització. El terme diversitat engloba múltiples facetes, ja que inclou informació taxonòmica, filogenètica o funcional sobre la singularitat evolutiva i ecològica dels organismes. A més, la diversitat té múltiples components perquè pot dividir-se en escales jeràrquiques (per exemple, escales espacials) formades per nivells (és a dir, α, β i γ). Mesurar simultàniament les tres facetes de la diversitat a diferents nivells d'una escala d'organització és necessari per a comprendre les regles que determinen la composició de la diversitat en una comunitat. No obstant això, altres definicions proposen incloure la força de les interaccions entre organismes o poblacions en la mesura de la diversitat, ja que els patrons d'interaccions entre organismes també poden produir variabilitat mesurable entre comunitats. L'estudi de les comunitats de paràsits sempre haja romàs darrere de l'ecologia de comunitats general, a pesar que els paràsits són ubics en tots els ecosistemes, el parasitisme és l'estratègia de vida més estesa entre les espècies existents i els paràsits juguen un paper clau en els processos ecològics. Atribuïsc aquest fet a dues causes principals. Primer, la forma de vida paràsita dificulta la quantificació dels efectes d'aquests organismes en la comunitat. En segon lloc, els parasitòlegs, generalment, han adoptat un enfocament descriptiu, malgrat els beneficis d'avançar cap a una ciència predictiva. Aquesta tesi doctoral té com a objectiu ampliar el nostre coneixement sobre l'ecologia de comunitats de paràsits, amb especial atenció a les comunitats de paràsits helmints de les llises (Teleostei: Mugilidae). No sols aprofitaré les últimes metodologies analítiques i tècniques d'ecologia de comunitats general, sinó que també adaptaré i optimitzaré el seu ús per a les comunitats d'organismes de vida lliure a l'ús en comunitats d'organismes paràsits. M'enfocaré en l'estudi de la diversitat de paràsits i les dinàmiques hoste-paràsit mitjançant l'índex de diversitat de Rao i l'anàlisi de xarxes bipartides. Amb aquests objectius en ment, he arribat a les següents conclusions. Primer, els mètodes basats en el modelatge d'argila i l'anàlisi d'imatges desenvolupats en el Capítol 3 per a estimar la massa d'organismes de mida xicoteta van ser precisos i no diferien significativament dels mètodes directes. Mentre que l'enfocament tradicional d'aproximació geomètrica va sobreestimar la massa. En conseqüència, recomane abandonar el seu ús. En segon lloc, espere que el marc teòric i la llista de set trets funcionals presentats en el Capítol 4 ajuden en estudis futurs a desvetllar preguntes ecològiques i evolutives en parasitologia. A més, espere que facilite als ecòlegs la inclusió dels paràsits en els seus estudis de comunitats. Tercer, aprofitant els mètodes (Capítol 3) i les consideracions teòriques (Capítol 4), en el Capítol 5 he trobat que la diversitat de les comunitats de paràsits de les llises de la Mediterrània occidental depén del nivell d'anàlisi i la faceta de la diversitat considerada. Per tant, les comunitats de paràsits no es poden entendre completament si alguna de les facetes de la diversitat es deixa de banda en un estudi de comunitats. Quart, en el Capítol 6 trobe que els individus de llises de dues espècies exerceixen funcions diferents per a les seues comunitats de paràsits depenent de la seua condició nativa o invasora i de les característiques de la comunitat de paràsits considerada. Propose que el seguiment a llarg termini de les funcions dels hostes invasors per a les comunitats de paràsits pot ser un indicador útil per a estimar la maduresa de l'establiment d'hostes invasors en un ecosistema. En general, aquesta tesi mostra com les comunitats de paràsits poden estudiar-se d'acord amb la teoria d'ecologia de comunitats actual. Aquesta tesi, ofereix noves eines als parasitòlegs per a millorar la seua comprensió del paper dels paràsits en els ecosistemes i espere que anime als ecòlegs a considerar els paràsits en els seus estudis per a obtindre una comprensió més àmplia dels processos dels ecosistemes. //Los organismos y las poblaciones en una localidad componen una comunidad biológica. La composición de poblaciones en una comunidad puede verse influenciada por procesos estocásticos o deterministas. Generalmente esta depende del nivel al que se estudie la comunidad. Para determinar las reglas que determinan la composición de la comunidad, debemos medir características significativas a nivel de comunidad ecológica, como la diversidad de la comunidad. La diversidad es la variabilidad de la vida en una localidad. El término diversidad engloba múltiples facetas, ya que incluye información taxonómica, filogenética o funcional sobre la singularidad evolutiva y ecológica de los. Además, la diversidad tiene múltiples componentes porque puede dividirse en escalas jerárquicas (por ejemplo, escalas espaciales) compuestas por niveles (es decir, α, β y γ). Medir simultáneamente las tres facetas de la diversidad a diferentes niveles de una escala de organización es relevante para comprender las reglas que determinan la composición de la diversidad en una comunidad. Sin embargo, otras definiciones proponen incluir la fuerza de las interacciones entre organismos o poblaciones en la medida de la diversidad, ya que los patrones de interacciones entre organismos también pueden producir variabilidad medible entre comunidades. El estudio de las comunidades de parásitos siempre se ha quedado retrasado con respecto a la ecología general de comunidades, a pesar de que los parásitos son ubicuos en todos los ecosistemas, el parasitismo es la estrategia de vida más extendida entre las especies existentes y los parásitos juegan un papel clave en los procesos ecológicos. Atribuyo este hecho a dos causas principales. Primero, la forma de vida parásita dificulta la cuantificación de los efectos de estos organismos en la comunidad. En segundo lugar, los parasitólogos, generalmente, han adoptado un enfoque descriptivo, a pesar de los beneficios de avanzar hacia una ciencia predictiva. Esta tesis doctoral tiene como objetivo ampliar nuestro conocimiento sobre la ecología de comunidades de parásitos, con especial atención a las comunidades de parásitos helmintos de los mújoles (Teleostei: Mugilidae). No solo aprovecharé las últimas metodologías analíticas y técnicas de ecología de comunidades general, sino que también adaptaré y optimizaré su uso para las comunidades de organismos de vida libre al uso en comunidades de organismos parásitos. Me enfocaré en el estudio de la diversidad de parásitos y las dinámicas hospedador-parásito mediante el índice de diversidad de Rao y el análisis de redes bipartitas. Con estos objetivos en mente, he llegado a las siguientes conclusiones. Primero, los métodos basados en el modelado de arcilla y el análisis de imágenes desarrollados en el Capítulo 3 para estimar la masa de organismos pequeños fueron precisos y no diferían significativamente de los métodos directos, mientras que el enfoque tradicional de aproximación geométrica sobreestimó la masa. En consecuencia, recomiendo abandonar su uso. En segundo lugar, espero que el marco teórico y la lista de siete rasgos funcionales presentados en el Capítulo 4 ayuden en estudios futuros a revelar preguntas ecológicas y evolutivas en parasitología. Además, espero que facilite a los ecólogos la inclusión de los parásitos en sus estudios de comunidades. Tercero, aprovechando los métodos (Capítulo 3) y las consideraciones teóricas (Capítulo 4), en el Capítulo 5 he encontrado que la diversidad de las comunidades de parásitos de los mújoles del Mediterráneo occidental depende del nivel de análisis y la faceta de la diversidad. considerada. Por lo tanto, las comunidades de parásitos no pueden entenderse completamente si alguna de las facetas de la diversidad se obvia en un estudio. Cuarto, en el Capítulo 6 concluyo que los individuos de mújoles de dos especies desempeñan funciones diferentes para sus comunidades de parásitos dependiendo de su estado nativo o invasor y de las características de la comunidad de parásitos considerada. Propongo que el seguimiento a largo plazo de las funciones de los hospedadores invasores para las comunidades de parásitos puede ser un indicador útil para estimar la madurez del establecimiento de hospedadores invasores en un ecosistema. En general, esta tesis muestra cómo las comunidades de parásitos pueden estudiarse de acuerdo con la teoría de ecología de comunidades actual. Esta tesis, ofrece nuevas herramientas a los parasitólogos para mejorar su comprensión del papel de los parásitos en los ecosistemas y espero que anime a los ecólogos a considerar los parásitos en sus estudios para obtener una comprensión más amplia de los procesos de los ecosistemas.Organisms and populations at a place compose a biological community. The assemblage of populations in a community can be influenced by stochastic or deterministic processes. It generally depends on the level at which the community is studied. To ascertain the rules that manage the community composition, one should focus on measuring features meaningful at the community level, such as the diversity of the community. Diversity is the variability of life at a place. Diversity is multifaceted because it includes taxonomic, phylogenetic or functional information about the evolutionary and ecological histories of the organisms and populations. Furthermore, diversity has multiple components because it can be partitioned across hierarchical scales (e.g. spatial scales) composed by levels (i.e. α, β and γ). The simultaneous measurement of the three facets of diversity in combination with its measurement at different levels of an organisational scale is relevant to understand the composition of the diversity in a community. However, other definitions propose to include the strength of interactions among organisms or populations in the measurement of diversity, since the patterns of interactions among organisms can also produce measurable variability between communities. The study of parasite communities has always lagged behind general community ecology, even though parasites are ubiquitous in all ecosystems, parasitism is the most extended life strategy among extant species and parasites play key roles in ecological processes. I attribute this fact to two main causes. First, the parasitic lifestyle complicates the quantification of the effects of these organisms on the community. Second, parasitologists have commonly adopted a descriptive approach, despite the unrivaled benefits of moving forward a predictive science. This doctoral thesis aims to increase our knowledge of the community ecology of parasites, with special attention to the helminth parasite communities of grey mullets (Teleostei: Mugilidae). I will not only take advantage of the last analytical methodologies and techniques of general community ecology, but I will also adapt and optimise their use in communities of free-living organisms to organisms with parasitic life strategies. I will focus on the study of parasite diversity and host–parasite dynamics by means of Rao’s index of diversity and the bipartite network analysis. With these objectives in mind, I have reached the following conclusions. First, the two methods based on Clay Modelling and Image Analysis developed in Chapter 3 to estimate mass of small organisms were accurate and did not significantly differ from the direct methods, whereas the traditional Geometric Approximation approach overestimated mass. Consequently, I strongly recommend abandoning its use. Second, I expect that the theoretical framework and the core list of seven functional traits presented in Chapter 4 will help future researchers to unveil ecological and evolutionary questions in parasitology. Moreover, I hope it will facilitate ecologists to include parasites in their studies. Third, taking advantage of the methods (Chapter 3) and theoretical considerations (Chapter 4) I found in Chapter 5 that the diversity of the parasite communities from grey mullets from the Western Mediterranean is dependent on the level of the analysis and the facet of diversity considered. Thus, parasite communities cannot be fully understood if any of the facets of diversity is neglected in a study. Fourth, I conclude in Chapter 6 that grey mullet individuals of two species play different roles for their parasite communities regarding the native or invasive status of the host individuals and the characteristics of the parasite community considered. I propose that long-term monitoring of the roles of invasive hosts in parasite communities can be a useful proxy for estimating the maturity of the establishment of the invasive hosts in an ecosystem. Overall, this thesis shows how parasite communities can be studied under the light of the current community ecology theory. It gives novel tools to parasitologists to improve our understanding of the role of parasites in ecosystems and we expect it will encourage ecologists to consider parasites in their studies to get a broader comprehension of ecosystem processes

Evaluation of three methods for biomass estimation in small invertebrates, using three large disparate parasite species as model organisms

Invertebrate biomass is considered one of the main factors driving processes in ecosystems. It can be measured directly, primarily by weighing individuals, but more often indirect estimators are used. We developed two indirect and non-destructive approaches to estimate biomass of small invertebrates in a simple manner. The first one was based on clay modelling and the second one was based on image analysis implemented with open-source software. Furthermore, we tested the accuracy of the widely used geometric approximation method (third method). We applied these three different methods to three morphologically disparate model species, an acanthocephalan worm, a crustacean and a flatworm. To validate our indirect estimations and to test their accuracy, we weighed specimens of the three species and calculated their tissue densities. Additionally, we propose an uncomplicated technique to estimate thickness of individuals under a microscope, a required measurement for two of the three indirect methods tested. The indirect methods proposed in this paper provided the best approximation to direct measurements. Despite its wide use, the geometric approximation method showed the lowest accuracy. The approaches developed herein are timely because the recently increasing number of studies requiring reliable biomass estimates for small invertebrates to explain crucial processes in ecosystems

Beyond counting species : a new way to look at biodiversity

In modern ecology, the traditional diversity indices (usually of richness, abundance, and species evenness) have been highly revealing and useful for monitoring community and ecosystem processes. However, around two decades ago, a pioneering research team noticed that these indices did not completely resolve their open questions. Thus, they suggested changing the way biodiversity was measured. At its base, this new methodology considers the distance between species (in phylogenetic or functional terms) before subsequently applying the appropriate biodiversity indices. Including phylogenetic and functional elements in the evaluation of diversity allows us to approach the concept of biodiversity in a more comprehensive way

Phenotypic plasticity in haptoral structures of Ligophorus cephali (Monogenea: Dactylogyridae) on the flathead mullet (Mugil cephalus): A Geometric Morphometric Approach

Evaluating phenotypic plasticity in attachment organs of parasites can provide information on the capacity to colonise new hosts and illuminate evolutionary processes driving host specificity. We analysed the variability in shape and size of the dorsal and ventral anchors of Ligophorus cephali from Mugil cephalus by means of geometric morphometrics and multivariate statistics. We also assessed the morphological integration between anchors and between the roots and points in order to gain insight into their functional morphology. Dorsal and ventral anchors showed a similar gradient of overall shape variation, but the amount of localised changes was much higher in the former. Statistical models describing variations in shape and size revealed clear differences between anchors. The dorsal anchor/bar complex seems more mobile than the ventral one in Ligophorus, and these differences may reflect different functional roles in attachment to the gills. The lower residual variation associated with the ventral anchor models suggests a tighter control of their shape and size, perhaps because these anchors seem to be responsible for firmer attachment and their size and shape would allow more effective responses to characteristics of the microenvironment within the individual host. Despite these putative functional differences, the high level of morphological integration indicates a concerted action between anchors. In addition, we found a slight, although significant, morphological integration between roots and points in both anchors, which suggests that a large fraction of the observed phenotypic variation does not compromise the functional role of anchors as levers. Given the low level of genetic variation in our sample, it is likely that much of the morphological variation reflects host-driven plastic responses. This supports the hypothesis of monogenean specificity through host-switching and rapid speciation. The present study demonstrates the potential of geometric morphometrics to provide new and previously unexplored insights into the functional morphology of attachment and evolutionary processes of host¿parasite coevolution

Replication Data for: Native and invasive hosts play different roles in host-parasite networks

This file containes the host-by-parasite-species abundance matrix, environmental variables and host traits used in the study

Sensitivity of bipartite network analyses to incomplete sampling and taxonomic uncertainty

Bipartite network analysis is a powerful tool to study the processes structuring interactions in ecological communities. In applying the method, it is assumed that the sampled interactions provide an accurate representation of the actual community. However, acquiring a representative sample may be difficult as not all species are equally abundant or easily identifiable. Two potential sampling issues can compromise the conclusions of bipartite network analyses: failure to capture the full range of interactions (sampling completeness) and use of a taxonomic level higher than species to evaluate the network (taxonomic resolution). We asked how commonly used descriptors of bipartite antagonistic communities (modularity, nestedness, connectance, and specialization [H2 0 ]) are affected by reduced host sampling completeness, parasite taxonomic resolution, and their crossed effect, as they are likely to co-occur. We used a quantitative niche model to generate weighted bipartite networks that resembled natural host–parasite communities. The descriptors were more sensitive to uncertainty in parasite taxonomic resolution than to host sampling completeness. When only 10% of parasite taxonomic resolution was retained, modularity and specialization decreased by ~76% and ~12%, respectively, and nestedness and connectance increased by ~114% and ~345% respectively. The loss of taxonomic resolution led to a wide range of possible communities, which made it difficult to predict its effects on a given network. With regards to host sampling completeness, standardized nestedness, connectance, and specialization were robust, whereas modularity was sensitive (~30% decrease). The combination of both sampling issues had an additive effect on modularity. In communities with low effort for both sampling issues (50%–10% of sampling completeness and taxonomic resolution), estimators of modularity, and nestedness could not be distinguished from those of random assemblages. Thus, the categorical description of communities with low sampling effort (e.g., if a community is modular or not) should be done with caution. We recommend evaluating both sampling completeness and taxonomic certainty when conducting bipartite network analyses. Care should also be exercised when using nonrobust descriptors (the four descriptors for parasite taxonomic resolution; modularity for host sampling completeness) when sampling issues are likely to affect a dataset

Changes in native and introduced host-parasite networks

Introduced species can alter the dynamics and structure of a native community. Network analysis provides a tool to study host-parasite interactions that can help to predict the possible impact of biological invasions or other disturbances. In this study, we used weighted bipartite networks to assess differences in the interaction patterns between hosts and helminth parasites of native (Sea of Japan) and invasive (Black Sea and Sea of Azov) populations of Planiliza haematocheilus (Teleostei: Mugilidae). We employed three quantitative network descriptors, connectance, weighted nestedness and modularity, to gain insight into the structure of the host-parasite networks in the native and invaded areas. The role of parasite species in the networks was assessed using the betweenness centrality index. We analyzed networks encompassing the whole helminth community and subsets of species classified by their transmission strategy. The analyses were downscaled to host individual-level to consider intraspecific variation in parasite communities. We found significant differences between networks in the native and invaded areas. The latter presented a higher value of nestedness, which may indicate a co-occurrence between parasite species with many connections in the network and species with fewer interactions within the same individual-host. In addition, modularity was higher in the native area's networks than those of the invaded area, with subgroups of host individuals that interact more frequently with certain parasite species than with others. Only the networks composed of actively transmitted parasites and ectoparasites did not show significant differences in modularity between the Sea of Azov and the Sea of Japan, which could be due to the introduction of a part of the native community into the invaded environment, with a lower diversity and abundance of species. We show that network analysis provides a valuable tool to illuminate the changes that occur in host-parasite interactions when an invasive species and its parasite community are introduced into a new area.ISSN:1387-3547ISSN:1573-146

Phenotypic Buffering in a Monogenean: Canalization and Developmental Stability in Shape and Size of the Haptoral Anchors of Ligophorus cephali (Monogenea: Dactylogyridae)

Phenotypic variation results from the balance between sources of variation and counteracting regulatory mechanisms. Canalization and developmental stability are two such mechanisms, acting at two different levels of regulation. The issue of whether or not they act concurrently as a common developmental buffering capacity has been subject to debate. We used geometric morphometrics to quantify the mechanisms that guarantee phenotypic constancy in the haptoral anchors of Ligophorus cephali. Canalization and developmental stability were appraised by estimating inter- and intra-individual variation, respectively, in size and shape of dorsal and ventral anchors. The latter variation was estimated as fluctuating asymmetry (FA) between anchor pairs. The general-buffering-capacity hypothesis was tested by two different methods based on correlations and Principal Components Analyses of the different components of size and shape variation. Evidence for FA in the dorsal and ventral anchors in both shape and size was found. Our analyses supported the hypothesis of a general developmental buffering capacity. The evidence was more compelling for shape than for size and, particularly, for the ventral anchors than for the dorsal ones. These results are in line with previous studies of dactylogyrids suggesting that ventral anchors secure a firmer, more permanent attachment, whereas dorsal anchors are more mobile. Because fixation to the host is crucial for survival in ectoparasites, we suggest that homeostatic development of the ventral anchors has been promoted to ensure the morphological constancy required for efficient attachment. Geometric morphometrics can be readily applied to other host-monogenean models, affording not only to disentangle the effects ofcanalization and developmental stability, as shown herein, but to further partition the environmental and genetic components of the forme

Towards a unified functional trait framework for parasites

Trait-based research holds high potential to unveil ecological and evolutionary processes. Functional traits are fitness-related characteristics of individuals, which are measured at individual level and defined without using information external to the individual. Despite the usefulness of the functional approach to understand the performance of individuals in ecosystems, and parasitism being the most common life-history strategy on Earth, studies based on functional traits of parasites are still scarce. Since the choice of functional traits is a critical step for any study, we propose a core list of seven functional traits of metazoan parasites, related to three universal challenges faced by organisms (dispersal, establishment, and persistence), and give guidelines to define appropriate functional traits in future parasite community studies.This study was funded by MINECO-FEDER, EU (CGL201571146-P), and the Swiss National Sci-ence Foundation (SNSF Grant No. 31003A_169211/1). This study is part of the PhD thesis of C.L.B.supported by Conselleria d’Educació, Investigació, Cultura i Esport (Generalitat Valenciana, Spain) and the European Social Fund (FSE) (contract number: ACIF/2016/37

Using network analysis to study and manage human-mediated dispersal of exotic species

Human-mediated dispersal is a major contributor of biological invasions. To reduce impacts induced by the introduction and spread of exotic species, biosecurity interventions are put into place. These interventions often rely on risk-assessment procedures, whereby biosecurity practitioners (which includes researchers, stakeholders such as national park managers, and all other decision makers who determine when and how to protect biodiversity) attempt to preemptively identify and predict which exotic species could potentially become a threat to natural ecosystems. In theory, extensive field and experimental studies would be required to accurately and precisely determine the risks of biological invasion of a species or group of species. However, due to a lack of resources or knowledge, such critical studies are limited. As a result, biosecurity practitioners rarely have a full picture of the extent to which the exotic species has and will spread at the time of decision making. Hence, they instead opt for preventive measures such as identifying and managing potential target exotic species which are likely to be invasive or dispersal pathways through which exotic species are likely to be introduced and spread. As most of the uncertainties pertaining to biosecurity interventions lie in the resolution of data made available to practitioners at the time of decision making, we first present some of the different types of information which are readily available during the risk-assessment procedure. We then highlight how one could exploit these different resolutions of data during the risk-assessment procedure using network analysis to better understand human-mediated dispersal of exotic species. By doing so, our paper puts forward what network analysis has to offer practitioners in the context of biosecurity interventions.ISSN:1387-3547ISSN:1573-146