Brian L. Fredensborg

Ecosystem energetic implications of parasite and free-living biomass in three estuaries

Parasites can have strong impacts but are thought to contribute little biomass to ecosystems. We quantified the biomass of free-living and parasitic species in three estuaries on the Pacific coast of California and Baja California. Here we show that parasites have substantial biomass in these ecosystems. We found that parasite biomass exceeded that of top predators. The biomass of trematodes was particularly high, being comparable to that of the abundant birds, fishes, burrowing shrimps and polychaetes. Trophically transmitted parasites and parasitic castrators subsumed more biomass than did other parasitic functional groups. The extended phenotype biomass controlled by parasitic castrators sometimes exceeded that of their uninfected hosts. The annual production of free-swimming trematode transmission stages was greater than the combined biomass of all quantified parasites and was also greater than bird biomass. This biomass and productivity of parasites implies a profound role for infectious processes in these estuaries.

DESCRIPTION AND PROPOSED LIFE CYCLE OF MARITREMA NOVAEZEALANDENSIS N. SP. (MICROPHALLIDAE) PARASITIC IN RED-BILLED GULLS, LARUS NOVAEHOLLANDIAE SCOPULINUS, FROM OTAGO HARBOR, SOUTH ISLAND, NEW ZEALAND

Maritrema novaezealandensis n. sp. is described from Otago Harbor, South Island, New Zealand, on the basis of adult specimens collected from the Red-billed gull, Larus novaehollandiae scopulinus, and excysted metacercariae obtained from crabs. It belongs to the “eroliae group” and differs from other related species mainly in the shape, size, and patterns of distributions of the spines on the cirrus, the shape of the metraterm, the presence of an unlobed ovary, and the complete ring of the vitelline follicles. Based on morphometric features of metacercariae and adult specimens, the trophic relationships among invertebrate and vertebrate hosts, experimental infections, and previous reports of species of Maritrema with similar transmission patterns, the life cycle of M. novaezealandensis n. sp. is described. A 3-host life cycle is proposed for this parasite. The first intermediate host is the mud snail, Zeacumantus subcarinatus, in which the cercarial stage is produced in sporocysts located within the gonad of the snail. At least 3 crab species (Hemigrapsus crenulatus, Macrophtalmus hirtipes, and Halicarcinus whitei) and several species of amphipods act as second intermediate hosts, with metacercariae encysted in the body cavity of the crustacean host. Finally, the definitive host, the gull, L. n. scopulinus, harbors the adult worms in its intestine.

The true cost of host manipulation by parasites.

If there is one thing that the past three decades of research in behavioural and evolutionary ecology have taught us, it is that there are no free lunches. Adaptive traits provide net fitness benefits to the animals bearing them, but the gains would be even greater if there were no concurrent costs associated with the expression of those traits. The ability of many parasites to enhance their transmission success by manipulating t 2 r a n m m T c e p I c F

Four trematode cercariae from the New Zealand intertidal snail Zeacumantus subcarinatus (Batillariidae)

Abstract The cercariae and sporocysts (or rediae) of four trematode species are described from the intertidal snail Zeacumantus subcarinatus: a distome xiphidiocercaria assigned to the genus Renicola (family Renicolidae); a monostome xiphidiocercaria belonging either to the genus Microphallus or Megalophallus (family Microphallidae); a magnacercous cercaria of the genus Galactosomum (family Hetero‐phyidae); and a cercaria of the genus Philophthalmus (family Philophthalmidae). The morphological features of these cercariae are compared to previously described cercariae of the same genera. In addition, since the philophthalmid cercaria encysts readily on artificial substrates in the laboratory, the metacercaria of this species is also described. These cercariae are part of a diverse community of at least six digenean species parasitising the snail Z. subcarinatus that, together, have a major impact on the ecology and evolution of this snail.

Food webs including parasites, biomass, body sizes, and life stages for three California/Baja California estuaries

This data set presents food webs for three North American Pacific coast estuaries and a “Metaweb” composed of the species/stages compiled from all three estuaries. The webs have four noteworthy attributes: (1) parasites (infectious agents), (2) body-size information, (3) biomass information, and (4) ontogenetic stages of many animals with complex life cycles. The estuaries are Carpinteria Salt Marsh, California (CSM); Estero de Punta Banda, Baja California (EPB); and Bahia Falsa in Bahia San Quintin, Baja California (BSQ). Most data on species assemblages and parasitism were gathered via consistent sampling that acquired body size and biomass information for plants and animals larger than ∼1 mm, and for many infectious agents (mostly metazoan parasites, but also some microbes). We augmented this with information from additional published sources and by sampling unrepresented groups (e.g., plankton). We estimated free-living consumer–resource links primarily by extending a previously published version of t...

Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages

The transmission stages of parasites are key determinants of parasite fitness, but they also incur huge mortality. Yet the selective forces shaping the sizes of transmission stages remain poorly understood. We ran a comparative analysis of interspecific variation in the size of transmission stages among 404 species of parasitic trematodes. There are two transmission steps requiring infective stages in the life cycle of trematodes: transmission from the definitive to the first intermediate (snail) host is achieved by eggs and/or the miracidia hatched from those eggs, and transmission from the first to the second intermediate host is achieved by free-swimming cercariae. The sizes of these stages are under strong phylogenetic constraints. Our results show that taxonomy explains >50% of the unaccounted variance in linear mixed models, with most of the variance occurring at the superfamily level. The models also demonstrated that mollusc size is positively associated with egg volume, miracidial volume and cercarial body volume, but not with the relative size of the cercarial tail. In species where they encyst on substrates, cercariae have significantly larger bodies than in species penetrating chordates, although the relative size of the cercarial tail of species using chordates as second intermediate hosts was larger than in other trematode species. Habitat also matters, with larger cercarial tails seen in freshwater trematodes than in marine ones, and larger miracidial volumes in freshwater species than in marine ones. Finally, the latitude (proxy for local temperature) at which the trematode species were collected had no effect on the sizes of transmission stages. We propose that resource availability within the snail host, the probability of contacting a host, and the density and viscosity of the water medium combine to select for different transmission stage sizes.

New records of gastrointestinal helminths from the red‐billed gull (Larus novaehollandiae scopulinus)

Abstract Eight species of gastrointestinal helminths were obtained from the red‐billed gull (Larus novaehollandiae scopulinus Forster, 1844) from Otago Peninsula, of which six were new host records. One of these, Maritrema novaezelandensis (Trematoda), was a species new to science which is being described elsewhere; the other five were Curtuteria australis (Trematoda), Echinoparyphium recurvatum (Trematoda), Cladogynia latovarium (Cestoda), Capillaria sp. (Nematoda), and Profilicollis novaezelandensis (Acanthocephala). Cladogynia latovarium (Cestoda) and Capillaria sp. (Nematoda) were present in 14 of the 16 birds.

DNA typing of ancient parasite eggs from environmental samples identifies human and animal worm infections in Viking-age settlement.

Abstract:  Ancient parasite eggs were recovered from environmental samples collected at a Viking-age settlement in Viborg, Denmark, dated 1018–1030 A.D. Morphological examination identified Ascaris sp., Trichuris sp., and Fasciola sp. eggs, but size and shape did not allow species identification. By carefully selecting genetic markers, PCR amplification and sequencing of ancient DNA (aDNA) isolates resulted in identification of: the human whipworm, Trichuris trichiura, using SSUrRNA sequence homology; Ascaris sp. with 100% homology to cox1 haplotype 07; and Fasciola hepatica using ITS1 sequence homology. The identification of T. trichiura eggs indicates that human fecal material is present and, hence, that the Ascaris sp. haplotype 07 was most likely a human variant in Viking-age Denmark. The location of the F. hepatica finding suggests that sheep or cattle are the most likely hosts. Further, we sequenced the Ascaris sp. 18S rRNA gene in recent isolates from humans and pigs of global distribution and show that this is not a suited marker for species-specific identification. Finally, we discuss ancient parasitism in Denmark and the implementation of aDNA analysis methods in paleoparasitological studies. We argue that when employing species-specific identification, soil samples offer excellent opportunities for studies of human parasite infections and of human and animal interactions of the past.

Increased Surfacing Behavior In Longnose Killifish Infected by Brain-Encysting Trematode

Abstract: Some parasites modify the behavior of intermediate hosts to increase the probability of transmission to the next host in their life cycle. In habitats where this is common, parasites play an important role in predator-prey links and food web dynamics. In this study we used laboratory observations to investigate the behavior of longnose killifish, Fundulus similis, that were naturally infected with metacercariae of the trematode, Euhaplorchis sp. A, from Laguna Madre, south Texas. In particular, we examined whether there was a relationship between the number of metacercariae lodged on the brain of the infected fish and behaviors that made the fish more conspicuous to avian final hosts. We also quantified the abundance and cercariae production of this parasite in its first intermediate snail host, Cerithidea pliculosa, and examined the seasonal variation of Euhaplorchis sp. A in F. similis. Our data demonstrated that Euhaplorchis sp. A affected the surfacing behavior of F. similis in an intensity-dependent manner. Fish with many infections spent longer time at the surface of the water than fish with few infections. Our data also show that Euhaplorchis sp. A is a common parasite in the first intermediate host and produces close to 4,000 cercariae m−2 day−1. Consequently 97% of all fish collected and necropsied were infected, with little seasonal variation in the mean abundance of the parasite. Based on our data, Euhaplorchis sp. A is likely important to predator-prey links in Gulf of Mexico estuary food webs, similar to the closely related Euhaplorchis californiensis in southern California. We expect that other closely related species elsewhere may have similar effects on other fish hosts, emphasizing the need for incorporating trophically transmitted parasites in estuarine food web studies.

A Gastropod Scavenger Serving as Paratenic Host for Larval Helminth Communities in Shore Crabs

The whelk Cominella glandiformis is an important predator–scavenger of New Zealand intertidal ecosystems; a few whelks can quickly eat all the soft tissues of recently dead crabs. In this study, we demonstrate that whelks can also ingest and act as paratenic hosts for at least 4 helminth species that use crabs as intermediate hosts: metacercariae of the trematode Maritrema sp. and of another unidentified trematode, larval acuariid nematodes, and cystacanths of the acanthocephalans Profilicollis spp. Large whelks ingest disproportionately more helminth larvae than small whelks, but the survival of parasites during their short stay in the whelks is not affected by whelk size. The majority of metacercariae and nematodes are passed out in whelk feces within 3 days of ingestion, whereas the few cystacanths found did not leave whelks until after that time; no parasite was left in whelks 5 days postingestion. Survival of all 4 helminth species was generally very high, though it decreased day by day in 2 species. Given that the avian definitive hosts of all 4 helminths also eat whelks, our results indicate that alternative transmission pathways exist and that parasites can take routes through food webs that are too often ignored.