Ciliary feeding structures and particle capture mechanism in the freshwater bryozoan Plumatella repens (Phylactolaemata)

Abstract. In contrast to marine bryozoans, the lophophore structure and the ciliary filter‐feeding mechanism in freshwater bryozoans have so far been only poorly described. Specimens of the phylactolaemate bryozoan Plumatella repens were studied to clarify the tentacular ciliary structures and the particle capture mechanism. Scanning electron microscopy revealed that the tentacles of the lophophore have a frontal band of densely packed cilia, and on each side a zigzag row of laterofrontal cilia and a band of lateral cilia. Phalloidin‐linked fluorescent dye showed no sign of muscular tissue within the tentacles. Video microscopy was used to describe basic characteristics of particle capture. Suspended particles in the incoming water flow, set up by the lateral ‘pump’ cilia on the tentacles, approach the tentacles with a velocity of 1–2 mm s^‐1. Near the tentacles, the particles are stopped by the stiff sensory laterofrontal cilia acting as a mechanical sieve, as previously seen in marine bryozoans. The particle capture mechanism suggested is based on the assumed ability of the sensory stiff laterofrontal cilia to be triggered by the deflection caused by the drag force of the through‐flowing water on a captured food particle. Thus, when a particle is stopped by the laterofrontal cilia, the otherwise stiff cilia are presumably triggered to make an inward flick which brings the restrained particle back into the downward directed main current, possibly to be captured again further down in the lophophore before being carried to the mouth via the food groove. No tentacle flicks and no transport of captured particles on the frontal side of the tentacles were observed. The velocity of the metachronal wave of the water‐pumping lateral cilia was measured to be ～0.2 mm s^‐1, the wavelength was ～7 μm, and hence the ciliary beat frequency estimated to be ～30 Hz (～20 °C). The filter feeding process in P. repens reported here resembles the ciliary sieving process described for marine bryozoans in recent years, although no tentacle flicks were observed in P. repens. The phylogenetic position of the phylactolaemates is discussed in the light of these findings.     

Feeding behavior in freshwater bryozoans: function,form, and flow

Bryozoans are impressively active suspension feeders, with diverse feeding behaviors. These have been studied extensively in marine bryozoans, but less so in their freshwater counterparts. Here we identified 16 distinct behaviors in three phylactolaemate species and classified them into behaviors involving separate tentacles, groups of tentacles, lophophore arms, the introvert, or multiple zooids. We examined (1) the repertoire of behaviors in each species, and each behavior's (2) absolute frequency, (3) relative frequency and (4) duration in each of the three species, at two flow velocities (0 and 0.2 cm s^?1). Nine feeding behaviors were shared by all three species, but the occurrence of other behaviors in a given species was limited by its morphology. Behaviors involved in particle capture were the most frequent, and were often faster than the reactions involved in particle rejection. By contrast, the absolute frequency of behaviors varied widely among species without clear associations with species form, or function of the behavior. Flow velocity had only minor effects on the feeding behaviors exhibited by a species, or their frequencies or durations. Our results show that phylactolaemates have the same key feeding behaviors of the individual polypides (especially involving separate tentacles) as previously described in gymnolaemate and stenolaemate bryozoans, although their behaviors tend to be carried out more slowly than those of stenolaemates or gymnolaemates. Feeding behaviors involving multiple zooids were nearly absent in the studied phylactolaemates, but are common in gymnolaemates. Freshwater bryozoans appear to be intermediate between stenolaemate and gymnolaemate bryozoans in terms of richness of the repertoire of feeding behaviors.     

Organogenesis during budding and lophophoral morphology of Hislopia malayensis Annandale, 1916 (Bryozoa, Ctenostomata)

Background  

Bryozoans represent a large lophotrochozoan phylum with controversially discussed phylogenetic position and in group relationships. Developmental processes during the budding of bryozoans are in need for revision. Just recently a study on a phylactolaemate bryozoan gave a comprehensive basis for further comparisons among bryozoans. The aim of this study is to gain more insight into developmental patterns during polypide formation in the budding process of bryozoans. Particular focus is laid upon the lophophore, also its condition in adults. For this purpose we studied organogenesis during budding and lophophoral morphology of the ctenostome bryozoan Hislopia malayensis.     

Organogenesis in the budding process of the freshwater bryozoan Cristatella mucedo Cuvier, 1798 (bryozoa,phylactolaemata)

The phylogenetic position of bryozoans has been disputed for decades, and molecular phylogenetic analyzes have not unequivocally clarified their position within the Bilateria. As probably the most basal bryozoans, Phylactolaemata is the most promising taxon for large‐scale phylogenetic comparisons. These comparisons require extending the morphological and developmental data by investigating different phylactolaemate species to identify basal characters and resolve in‐group phylogeny. Accordingly, we analyzed the bud development and the organogenesis of the freshwater bryozoan Cristatella mucedo, with special focus on the formation of the digestive tract and differentiation of the coelomic compartments. Most parts of the digestive tract are formed as an outpocketing at the future anal side growing towards the mouth area. The ganglion is formed by an invagination between the anlagen of the mouth and anus. The lophophoral arms develop as paired lateral protrusions into the lumen of the bud and are temporarily connected by a median, thin bridge. All coelomic compartments are confluent during their development and also in the adult. The epistome coelom develops by fusion of two peritoneal infolds between the gut loop and overgrows the ganglion medially. The coelomic ring canal on the oral side develops by two lateral ingrowths and supplies the oral tentacles. On the forked canal, supplying the innermost row of tentacles above the epistome, a bladder‐shaped swelling, probably with excretory function, is present in some adults. It remains difficult to draw comparisons to other phyla because only few studies have dealt with budding of potentially related taxa in more detail. Nonetheless, our results show that comparative organogenesis can contribute to phylactolaemate systematics and, when more data are available, possibly to that of other bryozoan classes and bilaterian phyla. J. Morphol., 2011. © 2010 Wiley‐Liss, Inc.     

A model of particle capture by bryozoans in turbulent flow: significance of colony form

A hydrodynamic model was developed to examine particle capture by lophophores of encrusting bryozoans. Particle capture rate is predicted to increase with increasing speed of the feeding current. There should be a large feeding advantage when lophophores are tightly packed and excurrents are vented through chimneys. This prediction contradicts conclusions of an earlier model study and suggests that selection for colony integration has a basis in the acquisition of food. If lophophores are not tightly packed, particle-capture patterns depend on two key ratios: the advection ratio (feeding current velocity to shear velocity) and the separation ratio (lophophore spacing to lophophore diameter). At high separation ratios, particle capture rates should be fairly uniform among zooids. At high advection ratios, lophophores located near the upstream colony edge should experience higher rates of particle capture. Rates of particle capture in turbulent flows should greatly exceed those in laminar flows (of identical speed) when excurrent waters are locally remixed into the flow above lophophores. However, when lophophores are tightly packed and excurrents are vented through chimneys, feeding rates should be identical in turbulent and laminar flows. Thus, colonies that vent excurrents through chimneys may be uniquely able to exploit weak laminar flows.     

Modern Data on the Innervation of the Lophophore in Lingula anatina (Brachiopoda) Support the Monophyly of the Lophophorates

Evolutionary relationships among members of the Lophophorata remain unclear. Traditionally, the Lophophorata included three phyla: Brachiopoda, Bryozoa or Ectoprocta, and Phoronida. All species in these phyla have a lophophore, which is regarded as a homologous structure of the lophophorates. Because the organization of the nervous system has been traditionally used to establish relationships among groups of animals, information on the organization of the nervous system in the lophophore of phoronids, brachiopods, and bryozoans may help clarify relationships among the lophophorates. In the current study, the innervation of the lophophore of the inarticulate brachiopod Lingula anatina is investigated by modern methods. The lophophore of L. anatina contains three brachial nerves: the main, accessory, and lower brachial nerves. The main brachial nerve is located at the base of the dorsal side of the brachial fold and gives rise to the cross neurite bundles, which pass through the connective tissue and connect the main and accessory brachial nerves. Nerves emanating from the accessory brachial nerve account for most of the tentacle innervation and comprise the frontal, latero-frontal, and latero-abfrontal neurite bundles. The lower brachial nerve gives rise to the abfrontal neurite bundles of the outer tentacles. Comparative analysis revealed the presence of many similar features in the organization of the lophophore nervous system in phoronids, brachiopods, and bryozoans. The main brachial nerve of L. anatina is similar to the dorsal ganglion of phoronids and the cerebral ganglion of bryozoans. The accessory brachial nerve of L. anatina is similar to the minor nerve ring of phoronids and the circumoral nerve ring of bryozoans. All lophophorates have intertentacular neurite bundles, which innervate adjacent tentacles. The presence of similar nerve elements in the lophophore of phoronids, brachiopods, and bryozoans supports the homology of the lophophore and the monophyly of the lophophorates.     

Global diversity of bryozoans (Bryozoa or Ectoprocta) in freshwater

The present study considers 88 bryozoan species occurring in freshwater: 69 phylactolaemate and 19 gymnolaemate species. Roughly 49% of these species are confined to one zoogeographical region. The cosmopolitan status of species like Fredericella sultana, Plumatella repens or P. emarginata has to be reconsidered. Among the Phylactolaemata, which are phylogenetically older than the Gymnolaemata, the gelatinous species (Lophopodidae, Pectinatellidae, Cristatellidae) are more primitive than the branching tubular species (Plumatellidae, Fredericellidae). Guest editors: E. V. Balian, C. Lévêque, H. Segers & K. Martens Freshwater Animal Diversity Assessment     

Multizooidal Budding in Parasmittina trispinosa (Johnston) (Bryozoa,Cheilostomata)

Two principally different wall types occur in the bryozoan colony: Exterior walls delimiting the super-individual, the colony, against its surroundings and interior walls dividing the body cavity of the colony thus defined into units which develop into sub-individuals, the zooids. In the gymnolaemate bryozoans generally, whether uniserial or multiserial, the longitudinal zooid walls are exterior, the transverse (proximal and distal) zooid walls interior ones. The radiating zooid rows grow apically to form “tubes” each surrounded by exterior walls but subdivided by interior (transverse) walls. The stenolaemate bryozoans show a contrasting mode of growth in which the colony swells in the distal direction to form one confluent cavity surrounded by an exterior wall but internally subdivided into zooids by interior walls. In the otherwise typical gymnolaemate Parasmittina trispinosa the growing edge is composed of a series of “giant buds” each surrounded by exterior walls on its lateral, frontal, basal and distal sides and forming an undifferentiated chamber usually 2–3 times as broad and 3 or more times as long as the final zooid. Its lumen is subdivided by interior walls into zooids 2–3, occasionally 4, in breadth. This type of zooid formation is therefore similar to the “common bud” or, better-named, “multizooidal budding” characteristic of the stenoleamates but has certainly evolved independently as a special modification of the usual gymnolaemate budding.     

Evidence from Hox genes that bryozoans are lophotrochozoans

Bryozoans, or moss animals, are small colonial organisms that possess a suspension-feeding apparatus called a lophophore. Traditionally, this "phylum" has been grouped with brachiopods and phoronids because of the feeding structure. Available molecular and morphological data refute this notion of a monophyletic "Lophophorata." Alternative hypotheses place bryozoans either at the base of the Lophotrochozoa or basal to the Lophotrochozoa/Ecdysozoa split. Surprisingly, the only molecular data bearing on this issue are from the 18S nuclear ribosomal gene. Here we report the results of a Hox gene survey using degenerate polymerase chain reaction primers in a gymnolaemate bryozoan, Bugula turrita. Putative orthologs to both the Post2 and the Lox5 genes were found, suggesting that bryozoans are not a basal protostome group but closely allied to other lophotrochozoan taxa. We also found the first definitive evidence of two Deformed/Hox4 class genes in a nonvertebrate animal.     

The mussel filter–pump – present understanding,with a re‐examination of gill preparations

Filter feeding in mussels is a secondary adaptation where the gills have become W‐shaped and greatly enlarged, acting as the mussel filter–pump. Water pumping and particle capture in the blue mussel, Mytilus edulis, have been studied over many years. Here, we give a short status of the present understanding of ciliary structure and function of the mussel filter–pump, supplemented with new photo‐microscope and scanning electron microscopy (SEM) pictures of gill preparations. Pumping rate (filtration) and pressure to maintain flow have been extensively studied so the power delivered by the mussel pump to the water flow is known (1.1% of total respiratory power), but the actual cost based on gill respiration is much higher (19%), implying that the cost of maintaining of the large gill pump is considerable and that only relatively little energy can be saved by stopping or reducing the activity of the water‐pumping cilia so that continuous feeding with a ‘minimal scaled’ pump is cheaper than discontinuous feeding with a correspondingly larger pump. According to the present view, the pump proper is the beating lateral cilia (lc) on the gill filaments and particle capture is accomplished by the action of laterofrontal cirri (lfc) transferring particles from the main water current to the frontal gill filament currents driven by frontal cilia (fc). Unexplained aspects include retention efficiency according to particle size and the role of pro‐laterofrontal cilia (p‐lfc) placed between the lfc and fc. The structure of cilia and the mode of ciliary beating have been re‐examined in this study by new high‐resolution light and scanning electron microscopy of isolated gill preparations exposed to serotonin (5‐HT) stimulation which can activate the lc and lfc at low concentrations (10^?6 M), but removes the lfc from the interfilament canals at higher concentrations (10^?5 M).     

Key novelties in the evolution of the aquatic colonial phylum Bryozoa: evidence from soft body morphology

Molecular techniques are currently the leading tools for reconstructing phylogenetic relationships, but our understanding of ancestral, plesiomorphic and apomorphic characters requires the study of the morphology of extant forms for testing these phylogenies and for reconstructing character evolution. This review highlights the potential of soft body morphology for inferring the evolution and phylogeny of the lophotrochozoan phylum Bryozoa. This colonial taxon comprises aquatic coelomate filter‐feeders that dominate many benthic communities, both marine and freshwater. Despite having a similar bauplan, bryozoans are morphologically highly diverse and are represented by three major taxa: Phylactolaemata, Stenolaemata and Gymnolaemata. Recent molecular studies resulted in a comprehensive phylogenetic tree with the Phylactolaemata sister to the remaining two taxa, and Stenolaemata (Cyclostomata) sister to Gymnolaemata. We plotted data of soft tissue morphology onto this phylogeny in order to gain further insights into the origin of morphological novelties and character evolution in the phylum. All three larger clades have morphological apomorphies assignable to the latest molecular phylogeny. Stenolaemata (Cyclostomata) and Gymnolaemata were united as monophyletic Myolaemata because of the apomorphic myoepithelial and triradiate pharynx. One of the main evolutionary changes in bryozoans is a change from a body wall with two well‐developed muscular layers and numerous retractor muscles in Phylactolaemata to a body wall with few specialized muscles and few retractors in the remaining bryozoans. Such a shift probably pre‐dated a body wall calcification that evolved independently at least twice in Bryozoa and resulted in the evolution of various hydrostatic mechanisms for polypide protrusion. In Cyclostomata, body wall calcification was accompanied by a unique detachment of the peritoneum from the epidermis to form the hydrostatic membraneous sac. The digestive tract of the Myolaemata differs from the phylactolaemate condition by a distinct ciliated pylorus not present in phylactolaemates. All bryozoans have a mesodermal funiculus, which is duplicated in Gymnolaemata. A colonial system of integration (CSI) of additional, sometimes branching, funicular cords connecting neighbouring zooids via pores with pore‐cell complexes evolved at least twice in Gymnolaemata. The nervous system in all bryozoans is subepithelial and concentrated at the lophophoral base and the tentacles. Tentacular nerves emerge intertentacularly in Phylactolaemata whereas they partially emanate directly from the cerebral ganglion or the circum‐oral nerve ring in myolaemates. Overall, morphological evidence shows that ancestral forms were small, colonial coelomates with a muscular body wall and a U‐shaped gut with ciliary tentacle crown, and were capable of asexual budding. Coloniality resulted in many novelties including the origin of zooidal polymorphism, an apomorphic landmark trait of the Myolaemata.     

Tentacle structure in freshwater bryozoans

Tentacles are the main food‐gathering organs of bryozoans. The most common design is a hollow tube of extracellular matrix (ECM), covered with ten columns of epithelial cells on the outside, and a coelothelium on the inside. Nerves follow the ECM, going between the bases of some epidermal cells. The tentacle musculature includes two bundles formed by myoepithelial cells of the coelothelium. The tentacles of freshwater (phylactolaemate) bryozoans, however, differ somewhat in structure from those of marine bryozoans. Here, we describe the tentacles of three species of phylactolaemates, comparing them to gymnolaemates and stenolaemates. Phylactolaemate tentacles tend to be longer, and with more voluminous coeloms. The composition of the frontal cell row and the number of frontal nerves is variable in freshwater bryozoans, but constant in marine groups. Abfrontal cells form a continuous row in Phylactolaemata, but occur intermittently in other two classes. Phylactolaemata lack the microvillar cuticle reported in Gymnolaemata. Abfrontal sensory tufts are always composed of pairs of mono‐ and/or biciliated cells. This arrangement differs from individual abfrontal ciliary cells of other bryozoans: monociliated in Stenolaemata and monociliated and multiciliated ones in Gymnolaemata. In all three groups, however, ciliated abfrontal cells probably serve as mechanoreceptors. We confirm previously described phylactolemate traits: an unusual arrangement of two‐layered coelothelium lining the lateral sides of the tentacle and oral slits in the intertentacular membrane. As previously reported, tentacle movements involved in feeding differ between bryozoan groups, with phylactolaemates tending to have slower movements than both gymnolaemates and stenolaemates, and a narrower behavioral repertoire than gymnolaemates. The morphological and ultrastructural differences between the freshwater species we studied and marine bryozoans may be related to these functional differences. Muscle organization, tentacle and coelom size, and degree of confluence between tentacle and lophophore coeloms probably account for much of the observed behavioral variability.     

A Simple and Highly Reproducible Technique to Extract the 14CO2 Resulting from Respiration of 14C-Labeled Seawater Samples

Plumatella geimermassardi is a newly recognized species of phylactolaemate bryozoan. Its known range extends from Ireland east through southern Norway and south into Italy. Colonies grow close to the substrate with little free branching; the body wall is mostly transparent and without an obvious raphe. Floatoblasts are broadly oval and relatively small, with distinctively large dorsal fenestra and uniformly narrow ventral annulus. The sessoblast basal valve is low and dish-shaped; the annulus bears tubercles which vary in their prominence. This species brings to 14 the number of phylactolaemate bryozoans known in the region.     

Enantiopure cyclic O‐substituted phenylphosphonothioic acid: Synthesis and chirality‐recognition ability

As a new acidic selector (resolving agent), we synthesized an enantiopure O‐alkyl phenylphosphonothioic acid with a seven‐membered ring ((R)‐ 5 ), which was designed on the basis of the results for the enantioseparation of 1‐arylethylamine derivatives with acyclic O‐ethyl phenylphosphonothioic acid ( I ). The phosphonothioic acid (R)‐ 5 showed unique chirality‐recognition ability in the enantioseparation of 1‐naphthylethylamine derivatives, aliphatic secondary amines, and amino alcohols; the ability was complementary to that of I . The X‐ray crystallographic analyses of the less‐ and more‐soluble diastereomeric salts showed that hydrogen‐bonding networks in the salt crystals are 2₁‐column‐type with a single exception which is cluster‐type. In the cases of the 2₁‐column‐type crystals, stability of the crystals is firstly governed by hydrogen bonds to form a 2₁‐column and secondly determined by intra‐columnar T‐shaped CH/π interaction(s), intra‐columnar hydrogen bond(s), inter‐columnar van der Waals interaction and/or inter‐columnar T‐shaped CH/π interaction(s). In contrast, the cluster‐type salt crystal is stabilized by the assistance of inter‐cluster T‐shaped CH/π and van der Waals interactions. To realize still more numbers of intra‐ and inter‐columnar and ‐cluster T‐shaped CH/π interactions, the seven‐membered ring of (R)‐ 5 plays a considerable role. Chirality 23:438–448, 2011. © 2009 Wiley‐Liss, Inc.     

The nervous system in the cyclostome bryozoan <Emphasis Type="Italic">Crisia eburnea</Emphasis> as revealed by transmission electron and confocal laser scanning microscopy

Introduction

Among bryozoans, cyclostome anatomy is the least studied by modern methods. New data on the nervous system fill the gap in our knowledge and make morphological analysis much more fruitful to resolve some questions of bryozoan evolution and phylogeny.

Results

The nervous system of cyclostome Crisia eburnea was studied by transmission electron microscopy and confocal laser scanning microscopy. The cerebral ganglion has an upper concavity and a small inner cavity filled with cilia and microvilli, thus exhibiting features of neuroepithelium. The cerebral ganglion is associated with the circumoral nerve ring, the circumpharyngeal nerve ring, and the outer nerve ring. Each tentacle has six longitudinal neurite bundles. The body wall is innervated by thick paired longitudinal nerves. Circular nerves are associated with atrial sphincter. A membranous sac, cardia, and caecum all have nervous plexus.

Conclusion

The nervous system of the cyclostome C. eburnea combines phylactolaemate and gymnolaemate features. Innervation of tentacles by six neurite bundles is similar of that in Phylactolaemata. The presence of circumpharyngeal nerve ring and outer nerve ring is characteristic of both, Cyclostomata and Gymnolaemata. The structure of the cerebral ganglion may be regarded as a result of transformation of hypothetical ancestral neuroepithelium. Primitive cerebral ganglion and combination of nerve plexus and cords in the nervous system of C. eburnea allows to suggest that the nerve system topography of C. eburnea may represent an ancestral state of nervous system organization in Bryozoa. Several scenarios describing evolution of the cerebral ganglion in different bryozoan groups are proposed.

     

Large‐scale ciliary reversal mediates capture of individual algal prey by Müller's larva

We documented capture of microalgal prey by several species of wild‐caught Müller's larvae of polyclad flatworms. To our knowledge, this is the first direct observation of feeding mechanism in this classical larval type. High‐speed video recordings showed that virtually all captures were mediated by large‐scale transient ciliary reversal over one or more portions of the main ciliary band corresponding to individual lobes or tentacles. Local ciliary beat reversals altered near‐field flow to suck parcels of food‐containing water mouthward. Many capture episodes entailed sufficient coordinated flow disruption that these compact‐bodied larvae tumbled dramatically. Similar behaviors were recorded in at least four distinct species, one of which corresponds to the ascidian‐eating polyclad Pseudoceros canadensis.     

Potential of high‐density pheromone‐releasing microtraps for control of codling moth Cydia pomonella and obliquebanded leafroller Choristoneura rosaceana

Recent large‐cage studies with codling moth Cydia pomonella (L.) reveal that the removal of moths from an apple orchard using pheromone‐releasing traps is more effective at reducing capture in a central monitoring trap than is a mating disruption protocol without kill/capture. The present study uses open orchard 0.2‐ha plots comparing a high‐density trapping scenario with mating disruption to confirm those results. Two tortricid moth pests of tree fruit are studied: codling moth and obliquebanded leafroller Choristoneura rosaceana (Harris). Codling moth treatments include Isomate CM FLEX (ShinEtsu Ltd, Japan), nonsticky traps baited with Trécé CM lures (Trécé, Inc., Adair, Oklahoma), and sticky traps baited with Trécé CM lures, all at equal application rates of 500 dispensers ha^?1, as well as a no pheromone control. These microtraps are of a novel design, small and easy to apply, and potentially inexpensive to produce. Mating disruption using Isomate CM FLEX and nonsticky traps reduces codling moth capture in standard monitoring traps by 58% and 71%, respectively. The attract‐and‐remove treatment with sticky traps reduces capture by 92%. Obliquebanded leafroller treatments include Isomate OBLR/PLR Plus and Pherocon IIB microtraps baited with Trécé OBLR lures, both applied at 500 dispensers ha^?1, as well as a no pheromone control. Mating disruption reduces capture in monitoring traps by 69%. The attract‐and‐remove treatment reduces capture by 85%. Both studies suggest that an attract‐and‐remove approach has the potential to provide superior control of moth populations compared with that achieved by mating disruption operating by competitive attraction.     

Host‐specific variation in off‐host performance of a temperate ectoparasite

Antagonistic host–parasite interactions are rarely considered from an ecological perspective of the parasite. We used a blood‐feeding ectoparasite of boreal cervids, the deer ked (Lipoptena cervi L., Hippoboscidae), to study host‐dependent variation in a parasite's ability to cope with an abiotic environment during the free‐living stage(s) in two allopatric Fennoscandian populations. We found that a strongly host‐specific deer ked population in eastern Fennoscandia, exploiting only moose (Alces alces), produced the largest offspring that were the most cold‐tolerant and emerged the earliest as adults, when compared with the western Fennoscandian population that exploited two hosts efficiently. Within the western population, however, offspring produced on roe deer (Capreolus capreolus) were significantly larger, more cold‐tolerant, and had higher survival than those produced on moose in the same area. We discuss potential causes for both host‐specific and geographical differences in off‐host performance: (1) maternal host directly affects the offspring survival prospects; (2) divergent co‐evolution with local main host(s) has shaped the parasite's life history; and/or (3) off‐host performance is shaped by adaptation to the local abiotic environment. In conclusion, this study increases our understanding of the evolution of host–parasite interactions by demonstrating how geographical differences in host exploitation may result in differences in survival prospects outside the host.