Host Burrows Research Articles

Within-host adaptive speciation of commensal yoyo clams leads to ecological exclusion, not co-existence.

Symbionts dominate planetary diversity and three primary symbiont diversification processes have been proposed: co-speciation with hosts, speciation by host-switching, and within-host speciation. The last mechanism is prevalent among members of an extraordinary marine symbiosis in the Indian River Lagoon, Florida, composed of a host mantis shrimp, Lysiosquilla scabricauda, and seven host-specific commensal vasconielline "yoyo" clams (Galeommatoidea) that collectively occupy two distinct niches: burrow-wall-attached, and host-attached/ectocommensal. This within-host symbiont radiation provides a natural experiment to test how symbiont coexistence patterns are regulated in a common ancestral habitat. The competitive exclusion principle predicts that sister taxa produced by adaptive speciation (with distinct morphologies and within-burrow niches) are most likely to coexist whereas the neutral theory predicts no difference among adaptive and non-adaptive sister taxa co-occurrence. To test these predictions, we engaged in (1) field-censusing commensal species assemblages; (2) trophic niche analyses; (3) laboratory behavioral observations. Although predicted by both models, the field census found no mixed-niche commensal assemblages: multi-species burrows were exclusively composed of burrow-wall commensals. Their co-occurrence matched random assembly process expectations, but presence of the single ectocommensal species had a highly significant negative effect on recruitment of all burrow-wall commensal species (P<0.001), including on its burrow-wall commensal sister species (P < 0.001). Our stable isotope data indicated that commensals are suspension feeders and that co-occurring burrow-wall commensals may exhibit trophic niche differentiation. The artificial burrow behavioral experiment yielded no evidence of spatial segregation among burrow-wall commensals, and it was terminated by a sudden breakdown of the host-commensal relationship resulting in a mass mortality of all commensals unattached to the host. This study system appears to contain two distinct, superimposed patterns of commensal distribution: (1) all burrow-wall commensal species; (2) the ectocommensal species. Burrow-wall commensals (the plesiomorphic condition) broadly adhere to neutral theory expectations of species assembly but the adaptive evolution of ectocommensalism has apparently led to ecological exclusion rather than coexistence, an inverse outcome of theoretical expectations. The ecological factors regulating the observed burrow-wall/ectocommensal exclusion are currently obscure but potentially include differential recruitment to host burrows and/or differential survival in "mixed" burrow assemblages, the latter potentially due to changes in host predatory behavior. Resampling host burrows during commensal recruitment peak periods and tracking burrow-wall commensal survival in host burrows with and without added ectocommensals could resolve this outstanding issue.

Snails riding mantis shrimps: Ectoparasites evolved from ancestors living as commensals on the host’s burrow wall

The molluscan class Gastropoda includes over 5,000 parasitic species whose evolutionary origins remain poorly understood. Marine snails of the genus Caledoniella (Caledoniellidae) are obligate parasites that live on the abdominal surface of the gonodactylid mantis shrimps. They have highly modified morphological characteristics specialized to the ectoparasitic lifestyle that make it difficult to infer their close relatives, thereby posing a question about their current systematic position in the superfamily Vanikoroidea. In the present study, we performed molecular phylogenetic analyses using three nuclear and three mitochondrial gene sequences to unveil the phylogenetic position of these enigmatic snails. The resulting trees recovered Caledoniella in the superfamily Truncatelloidea and within a subclade of commensal species that live on the burrow wall of marine benthic invertebrates. More specifically, Caledoniella formed the sister clade to a commensal snail species living in mantis-shrimp burrows and they collectively were sister to Sigaretornus planus (formerly in the family Tornidae or Vitrinellidae), a commensal living in echiuran burrows. This topology suggests that the species of Caledoniella achieved their ectoparasitic mode of life through the following evolutionary pathway: (1) invasion into the burrows of benthic invertebrates, (2) specialization to mantis shrimps, and (3) colonization of the host body surface from the host burrow wall with the evolution of the parasitic nature. The final step is likely to have been accompanied by the acquisition of a sucker on the metapodium, the loss of the radula and operculum, and the formation of monogamous pair bonds. The present molecular phylogeny also suggested parallel evolution of planispiral shells in a subclade of Truncatelloidea and enabled us to newly redefine the families Caledoniellidae, Elachisinidae, Teinostomatidae, Tornidae and Vitrinellidae.

Body size and ecological traits in fleas parasitic on small mammals in the Palearctic: larger species attain higher abundance.

We studied the relationships between body size and (a) abundance and (b) host specificity in fleas parasitic on small mammals (rodents and shrews) in the Palearctic taking into account the confounding effect of phylogeny. We tested these relationships both across 127 flea species and within separate phylogenetic clades, predicting higher abundance and lower host specificity (in terms of the number or diversity of hosts used by a flea) in smaller species. We also tested for the relationships between body size and abundance separately for species that spend most of their lives on a host's body (the "body" fleas) and species that spend most of their lives in a host's burrow or nest (the "nest" fleas). A significant phylogenetic signal in body size was detected across all fleas, as well as in five of six separate clades. Across all fleas and in majority of phylogenetic clades, mean abundance significantly increased with an increase in body size. The same pattern was found for both the "body" and the "nest" fleas, although the slope of the relationship appeared to be steeper in the former than in the latter. Neither measure of host specificity demonstrated a significant correlation with body size regardless of the subset of flea species analysed. We explain higher abundance attained by larger flea species by higher fecundity and/or competitive advantage upon smaller species at larval stage. We conclude that the macroecological patterns reported to date in parasites are far from being universal.

Airborne LiDAR and Aerial Imagery to Assess Potential Burrow Locations for the Desert Tortoise (Gopherus agassizii)

The Southwestern United States desert serves as the host for several threatened and endangered species, one of which is the desert tortoise (Gopherus agassizii). The goal of this study was to develop a fine-scale, remote-sensing-based approach that indicates favorable burrow locations for G. agassizii in the Boulder City (Nevada) Conservation Easement area (35,500 ha). This was done by analyzing airborne LiDAR data (5–7 points/m2) and color imagery (four bands, 0.15-m resolution) and determining the percent vegetation cover; shrub height and area; Normalized Difference Vegetation Index (NDVI); and several geomorphic characteristics including slope, azimuth, and roughness. Other field data used herein include estimates of canopy area and species richness using 1271 line transects, and shrub height and canopy area using plant-specific measurements of ~200 plants. Larrea tridentata and Ambrosia dumosa shrubs were identified using an algorithm that obtained an optimum combination of NDVI and average reflectance of the four bands (IR, R, G, and B) from pixels in each image. The results, which identified more than 65 million shrubs across the study area, indicate that percent vegetation cover from aerial imagery across the site (13.92%) compared favorably (14.52%) to the estimate obtained from line transects, though the LiDAR method yielded shrub heights approximately 60% those of measured shrub heights. Landscape and plant properties were combined with known locations of tortoise burrows, as visually observed in 2014. Masks were created using roughness coefficient, slope percent, azimuth of burrow openings, elevation, and percent vegetation cover to isolate areas more likely to host burrows. Combined, the masks isolated 55% of the total survey area, which will help target future field surveys. Overall, the approach provides areas where tortoise burrows are more likely to be found, though additional ecological data would help refine the overall method.

Borniopsis mortoni sp. n. (Heterodonta, Galeommatoidea, Galeommatidaesensu lato), a new bivalve commensal with a synaptid sea cucumber from Japan.

The Galeommatoidea is a bivalve superfamily that exhibits high species diversity in shallow waters. Many members of this superfamily are associated commensally with burrowing marine invertebrates in benthic sediments. The genus Borniopsis is known only from eastern Asia and exhibits high host diversity (e.g., mantis shrimps, crabs, holothurians, sipunculans and echiurans). A new species, Borniopsis mortoni sp. n., is described from mud flats at the mouth of the Souzu River, southwestern Shikoku Island, Japan. This species has elongate-ovate shells covered by a tan to dark brown periostracum, and lives attached by both its foot and byssal threads to the body surface of the synaptid sea cucumber Patinapta ooplax. Several individuals of Borniopsis mortoni are often found on the same host, but sometimes more than 10 individuals can occur together. Borniopsis mortoni is one of the smallest species in this genus. Probably, its small body size is an adaptation to the mode of life in a narrow host burrow. Until now, only two other Borniopsis species were known to have commensal associations with synaptids. Thus, this is the third example of a synaptid-associated species from this genus. In addition, we briefly review the galeommatoideans commensal with apodid sea cucumbers.

Symbiotic Association of the Bivalve Tellimya fujitaniana (Galeommatoidea) with the Heart Urchin Echinocardium cordatum (Spatangoida) in the Northwestern Pacific.

The bivalve Tellimya fujitaniana ( Yokoyama, 1927 ) (Galeommatoidea, Heterodonta) was described based on a fossil shell. Until now, the biology of living animals has not been reported. In this study, we found T. fujitaniana in a commensal relationship with the heart urchin Echinocardium cordatum (Pennant, 1777) (Spatangoida, Echinoidea) on the intertidal mud flats of the Seto Inland Sea, Japan. We investigated the morphology, host associations, and reproductive biology of this bivalve species. The elongate-ovate shell is covered by a reddish-brown ferruginous deposit. The mantle is exposed anteriorly to form a temporal siphon, while posteriorly one pair of short tentacles is exposed. Small individuals (shell length, SL, ≤ 2.1 mm) were attached to the host's body surface; middle-sized individuals (SL 3.0-3.2 mm) were attached to or stayed close to larger T. fujitanianathat were living freely in the host burrow. Nearly all the large individuals (SL ≥ 4.8 mm) lived freely in the host burrow, behind the urchin. This suggests that the host utilization pattern of T. fujitanianachanges with development. Specimens with SL ≥ 4.8 mm had mature gonads, mostly occupied by ova, and some individuals were brooding eggs or veliger larvae in the gills. This species was previously assigned to Fronsella. However, the morphology and ecology of this bivalve are very similar to those of Tellimya ferruginosa (the type species of the genus Tellimya) in the northeastern Atlantic Ocean. Thus, we have reassigned this species to genus Tellimya. We also confirmed that T. fujitaniana and T. ferruginosa can be genetically distinguished using the mitochondrial COI gene.

The enigmatic bivalve genus Paramya (Myoidea: Myidae): symbiotic association of an East Asian species with spoon worms (Echiura) and its transfer to the family Basterotiidae (Galeommatoidea)

Paramya is an enigmatic genus of Myidae (Bivalvia: Heterodonta: Myoidea) that includes three uncommon species: Paramya subovata (Conrad, 1845), Paramya recluzi (A. Adams, 1864) and Paramya africana Cosel, 1995. Paramya subovata is known as a commensal living in the burrow of the spoon worm Thalassema hartmani Fisher, 1947 (Annelida: Echiura: Thalassematidae), in North American coastal waters. However, the biology of the other two species remains unknown. In this study, we found P. recluzi living in the burrows of the two thalassematid echiuran species, Ikedosoma gogoshimense (Ikeda, 1904) and Arhynchite hayaoi Tanaka &amp; Nishikawa, 2013, in intertidal flats in the Seto Inland Sea, Japan. Paramya recluzi was embedded in the burrow wall with its short siphons protruding into the host burrow lumen for respiration and filter feeding. To determine the phylogenetic position of P. recluzi, we performed a molecular phylogenetic analysis using the 18S, 28S, COI and H3 genes. Molecular analysis showed that P. recluzi belongs not to the family Myidae, but to the genus Basterotia (Galeommatoidea: Basterotiidae). Morphological examination of P. recluzi revealed that this species has many similarities with Basterotia (e.g. a single cardinal tooth on each valve and short siphons surrounded by tentacles). Thus, we propose that this species should be transferred from the genus Paramya to Basterotia. In addition, we also suggest that the other two species of Paramya (P. subovata and P. africana) should be transferred to the family Basterotiidae based on their shell morphology, anatomy and ecological characteristics.

Observations on the life history of a rare shrimp, Salmoneus carvachoi (Crustacea: Caridea: Alpheidae), a possible simultaneous hermaphrodite

This study reports on the life history of a rare alpheid shrimp,Salmoneus carvachoi, in the tropical western Atlantic. At an intertidal flat in Pontal Bay, Ilhéus, Bahia, north-eastern Brazil,S. carvachoiwas collected from within burrows of the axianassid mud shrimpAxianassa australisand the caridean snapping shrimpsAlpheus estuariensisandAlpheus chacei. These and earlier studies that reportedS. carvachoiin dwellings constructed by other larger burrowing crustaceans suggest thatS. carvachoiis a generalist species that establishes facultative symbiotic partnerships with larger burrowing decapods. We collected a total of 52 individuals during the sampling period (1 year); 19 (36.5%) of these shrimps carried embryos underneath the abdomen. The mean ± SD carapace length was 4.7 ± 0.7 and 5.5 ± 0.3 mm in non-brooding and brooding shrimps, respectively. All collected specimens, whether or not brooding embryos, bear appendices masculinae on the endopods of the second pleopods. Burrows harboured only one or two shrimps and never three or more shrimps. Pairs of shrimp that inhabited burrows consisted of two brooding shrimps (N = 3 pairs), two non-brooding shrimps (N = 3), or one brooding and one non-brooding shrimp (N = 1). The presence of appendices masculinae in all collected shrimps, whether or not brooding embryos, and the pairing of brooding shrimp within host burrows suggest thatS. carvachoiis a simultaneously hermaphroditic species.

Sex ratio in flea infrapopulations: number of fleas, host gender and host age do not have an effect

This study set out to determine whether the sex ratio of fleas collected from host bodies is a reliable indicator of sex ratio in the entire flea population. To answer this question, previously published data on 18 flea species was used and it was tested to see whether a correlation exists between the sex ratio of fleas collected from host bodies and the sex ratio of fleas collected from host burrows. Across species, the female:male ratio of fleas on hosts correlated strongly with the female:male ratio of fleas in their burrows, with the slope of the regression overlapping 1. Controlling for flea phylogeny by independent contrasts produced similar results. It was also ascertained whether a host individual is a proportional random sampler of male and female fleas and whether the sex ratio in flea infrapopulations depends on the size of infrapopulations and on the gender and age of a host. Using field data, the sex ratio in infrapopulations of 7 flea species parasitic on 4 rodent species was analysed. Populations of 3 species (Nosopsyllus iranus, Parapulex chephrenis and Xenopsylla conformis) were significantly female-biased, whereas male bias was found in 1 species (Synosternus cleopatrae). In general, the sex ratio of fleas collected from an individual rodent did not differ significantly from the sex ratio in the entire flea population. Neither host gender, and age nor number of fleas co-occurring on a host affected (a) the sex ratio in flea infrapopulations and (b) the probability of an infrapopulation to be either female- or male-biased.

Simple epidemiological model predicts the relationships between prevalence and abundance in ixodid ticks

We tested whether the prevalence of ticks can be predicted reliably from a simple epidemiological model that takes into account only mean abundance and its variance. We used data on the abundance and distribution of larvae and nymphs of 2 ixodid ticks parasitic on small mammals (Apodemus agrarius, Apodemus flavicollis, Apodemus uralensis, Clethrionomys glareolus and Microtus arvalis) in central Europe. Ixodes trianguliceps is active all year round, occurs in the study area in the mountain and sub-mountain habitats only and inhabits mainly host burrows and nests, whereas Ixodes ricinus occurs mainly during the warmer seasons, occupies a large variety of habitats and quests for hosts outside their shelters. In I. ricinus, the models with k values calculated from Taylor's power law overestimated prevalences. However, if moment estimates of k corrected for host number were used instead, expected prevalences of both larvae and nymphs I. ricinus in either host did not differ significantly from observed prevalences. In contrast, prevalences of larvae and nymphs of I. trianguliceps predicted by models using parameters of Taylor's power law did not differ significantly from observed prevalences, whereas the models with moment estimates of k corrected for host number in some cases under-estimated relatively lower larval prevalences and over-estimated relatively higher larval prevalences, but predicted nymphal prevalences well.

Individual variation and prior experience affect the discrimination of a brood-parasite by its subsocial beetle host

In birds, host experience can modify response to parasites but nothing similar is known for insects. We studied two desert tenebrionid beetles, the subsocial host Parastizopus armaticeps and its obligate and ubiquitous brood-(clepto)parasite Eremostibes opacus, which mimics the host’s odour spectrum. Nearly 10% of host burrows in the field (n=214) remain unparasitised even after introducing E. opacus experimentally (n=22). In discrimination tests, 7% of naive host beetles eject the parasite, showing individual variation in olfactory discrimination ability. To test for effects of prior breeding experience, naive (“first time”) or experienced (“second time”) breeders with or without prior parasite contact were confined with E. opacus at breeding onset, their behaviour recorded and parasite number counted on breeding completion. More first- than second-time breeding pairs completely excluded the parasite and second-time breeders with no prior contact with E. opacus had fewer parasites than any others. These pairs increased burrow-guarding dramatically, mostly during early reproduction, this being the best predictor of parasite number. Prolonged guarding, however, must be traded-off against other brood-care behaviours. Hence, it might pay breeding pairs to take the risk of accepting some parasites breeding within their burrow, and we expect this effect will be more pronounced if poor feeding and digging conditions are taken into account. This might explain why apparently 90% of the P. armaticeps breeding burrows in the field contain at least one parasitic E. opacus.

Sampling fleas: the reliability of host infestation data.

The use of measures of host infestation as a reliable indicator of a flea population size to be used in interspecific comparisons was considered. The abundance of fleas collected from host bodies and collected from host burrows was compared among 55 flea species, controlling for the effect of flea phylogeny. The mean number of fleas on host bodies correlated positively with the mean number of fleas in host burrows/nests both when the entire data pool was analysed and for separate subsets of data on 'fur' fleas and 'nest' fleas. This was also true for a within-host (Microtus californicus) between-flea comparison. The results of this study demonstrate that, in general, the index of host body infestation by fleas can be used reliably as an indicator of the entire population size.

Seasonal abundance patterns of the sandfly Phlebotomus papatasi in climatically distinct foci of cutaneous leishmaniasis in Israeli deserts.

Among foci of cutaneous leishmaniasis in Israel, population densities of the vector sandfly Phlebotomus papatasi Scopoli (Diptera: Psychodidae) were assessed during April-October 1999 in the mesic Negev desert and the hyper-xeric Arava valley, using sticky traps placed overnight near host burrows of the fat sand rat, Psammomys obesus Cretzschmar (Cricetidae: Gerbillinae). Population dynamics of Ph. papatasi differed between the Negev (study sites on sand near Mount Keren and on loess at Nizzana ruins) and the Arava valley (study sites on sand at Shezaf and in a fallow field near irrigation at wadi Arava). At the Negev sites, sandfly abundance peaked in spring (April or May), whereas at Arava sites Ph. papatasi population densities were bi-modal, with peaks in both spring and autumn (September or October). This might be conducive to sustaining enzootic Leishmania major Yakimoff & Schokhor (Kinetoplastida: Trypanosomatidae). In both areas, Ph. papatasi densities were much higher at the site with moister soil, raising transmission risks of zoonotic cutaneous leishmaniasis.

The Biology of the Spider Wasp, Pepsis Thisbe (Hymenoptera:Pompilidae) From Trans Pecos, Texas. II. Temporal Patterns ofActivity and Hunting Behavior With Special Reference to theEffects of Experience

The temporal pattern of activity and hunting behavior of the spider wasp, Pepsis thisbe, from Trans Pecos, Texas are described. Females exhibited a bimodal pattern with peak periods of hunting activities occurring between 0800–0959 and 1600–1759 hr. The lowest levels of activity (1100–1359 hr) occurred when ambient temperatures exceeded 38℃. Activity declined abruptly after 1800 hr indicating a strong preference for diurnal activity in this species. The behavioral components of the hunting sequence consist of an initial approach and antennation of the host, grooming, antennation and paralyzation followed in some cases by lapping, ovipositiom burial of the host, and closure of the nest. The time required to complete the hunting sequence was recorded for both field and laboratory encounters between a wasp and spider. The amount of time required by a female wasp to complete the initial approach and antennation‐paralyzation sequences decreased significantly as a function of increasing encounter experience. The spider is stung most frequently (&gt;80%) through the intersegmental membrane between the sternum and coxa of the first leg. Whether or not a wasp exhibits lapping behavior is determined by the amount of time spent in flight searching for a host burrow.

Ecology and Behavior of Melecta separata callura (Hymenoptera: Anthophoridae)

Melecta separata callura (Cockerell), the primary biotic enemy of Anthophora edwardsii Cresson, behaves similarly to its European congeners, but differently from other North American parasitic melectine and nomadine bees. Features unique to Melecta (s. str.) include: digging through the soil plug of the completed host burrow; opening a small hole in the cap of the cell; ovipositing through this opening and attaching its egg to the roof or upper cell wall; resealing the cell; and replugging the host burrow. The bees spin a cocoon. They pupate in the autumn and overwinter as adults in the cells of their hosts. Melecta was parasitized by Sphaeropthalma unicolor (Cresson) and an undetermined bomblyiid fly. With the exception of a few host associations and flower records, there have been no studies on the ecology and behavior of any North American species of Melecta. Some features of the life history and interrelationships with host species have been worked out for the related Xeromelecta californica (Cresson) by Linsley and MacSwain (1942) and Porter (1951). These studies serve as a useful basis for comparisons between the two genera. In addition, a few studies on the ecology and behavior of European species of Melecta M. armata Panzer by Semichon (1904, 1911, 1922, 1925) and Malyshev (1928) and M. luctuosa Scopoli by Giordani-Soika (1936) provide a basis for intrageneric comparisons. Melecta (Melecta) separata callura (Cockerell) is a parasite of Anthophora edwardsii Cresson. The present study was conducted at a site near Coalinga and is; supplemented by unpublished 1947 observations made at a site near Somersville by Drs. E. G. Linsley, J. W. MacSwain and R. F. Smith. Thorp (1969) has discussed the ecology of the host bee, the habitats of the two sites where M. separata was studied, the temporal and spatial distribution of the two species, and has briefly outlined the ecology of the parasite. The present paper treats in more detail the behavior of the adult females. associated with oviposition, and the feeding behavior and development of the larvae of