Status of the Nemertea as prey in marine ecosystems

Nemerteans are predators of a wide variety of animals, but little is known of their role as prey for other animals. The presence of toxins in the tissues and secretions of these worms has led to the assumption usually suggested that they are ingested only rarely. However, analysis of a Food Habits Data Base from the United States National Marine Fisheries Service, compiled for fishes collected in the Atlantic Ocean from the Canadian border to Cape Hatteras, North Carolina (1973–1990), showed that nemerteans were recovered from the stomachs of 27 species of fishes in 14 families. They were found in 223 of 26 642 (0.84%) fish stomachs examined in the laboratory, but only in 0.09% of 58 812 fish examined in the field. Among species in the former category, for which 1000 were examined, the winter flounder, Pseudopleuronectes americanus(Walbaum), and the yellowtail flounder, Limanda ferruginea (Storer), had the greatest frequency of nemerteans, 71 of 1545 (4.6%) and 33 of 1045 (3.2%), respectively. These nemerteans were identified as Nemertea, Cerebratulus sp. or Micrura sp., but it is likely that they were all of a Cerebratulus-like type. Nemerteans have also been recorded from the guts of eight additional species (including four additional families) of fishes collected from the western Atlantic Ocean, Gulf of Mexico, eastern Pacific Ocean (Washington, Alaska), North Sea and Indian Ocean off South Africa. The black-bellied plover, Pluvialis squatarola(L.), semipalmated plover, Charadrius semipalmatus Bonapart and the herring gull, Larus argentatus Pontoppidan are the only three species known to feed on nemerteans (Cerebratulus lacteus (Leidy) and Paranemertes peregrina Coe by the black-bellied plover and C. lacteus by the other species). Several species of nemerteans are known to ingest other nemerteans, and several arthropods, a squid, and a few other invertebrates also feed on these worms. On the other hand, careful laboratory studies have shown that some members of the Palaeonemertea, Heteronemertea and Hoplonemertea, when fed to various species of fishes, crustaceans (Astacidea, Anomura, Brachyura and Amphipoda) and a polychaete, were rejected, usually violently. There is a history of using large nemerteans, e.g. Cerebratulus lacteus and Polybrachiorhynchus dayi, as bait by sport fishermen in the United States and South Africa. The incongruity of successfuly using these toxic animals to catch fish is discussed in relation to conclusions on the importance of nemerteans as prey in the marine environment.     

Feeding rates of the nemertean Prosorhochmus americanus (Hoplonemertea) on two species of gammaridean amphipods

Abstract. The intertidal hoplonemertean Prosorhochmus americanus is a common inhabitant of the fouling community of rock jetties of the southeast coast of the United States. We undertook a laboratory investigation of the feeding rate of this nemertean, which is a suctorial predator of amphipod crustaceans that co‐occur in abundance in the fouling community. While submerged in water (simulating high tide), worms fed on the tube‐building amphipods Jassa falcata and Corophium cf. insidiosum at rates of 0.19 amphipods nemertean^?1 d^?1 (n=10) and 0.26 amphipods nemertean^?1 d^?1 (n=14), respectively. These predation rates were not significantly different (two‐tailed t‐test, p>0.05), and are similar to those estimated in laboratory studies of other suctorial nemerteans. Many nemerteans are typically more active at night, and indeed, adults of P. americanus consumed more individuals of J. falcata during dark periods than during light periods (χ² analysis, p<0.05). However, no difference in consumption of individuals of C. cf. insidiosum was observed in dark versus light. We attribute these contrasting results to differences in tube‐building behavior exhibited by these two species of amphipod under laboratory conditions. Our results and those of other laboratory investigations suggest that nemerteans that prey on amphipods feed at a rate of ～0.2 prey items nemertean^?1 d^?1, but under natural conditions this rate may not be obtained because of limited feeding time, longer foraging distances, and emigration of prey from regions of high nemertean activity.     

Predation rates of nemertean predators: the case of a rocky shore hoplonemertean feeding on amphipods

Estimates of the predation rates of benthic nemerteans are often based on observations of single individuals, and consequently they may not be representative for all members of a population of these predators. Herein we conducted controlled and repeatable laboratory experiments on the predation rate of the hoplonemertean Amphiporus nelsoni Sánchez 1973, which is common at exposed rocky shores along the central Chilean coast. During the austral fall (April, May 2000), nemerteans were observed in relatively high numbers crawling in the intertidal zone during early morning or late-afternoon low tides. When these nemerteans were offered living amphipods held by a forceps, they immediately attacked the amphipods and fed on them. In the laboratory experiments, nemerteans preferred the amphipod Hyale maroubrae Stebbing, 1899, which is also very common in the natural habitat of A. nelsoni. The nemerteans preyed to a higher extent on small males and non-ovigerous females than would have been expected from their abundance. We suggest that these (non-reproductive) stages of H. maroubrae are very mobile and therefore have a high likelihood of encounters with nemerteans. Predation rates reached maxima when nemerteans were provided prey densities of four or more of their preferred prey species, H. maroubrae, furthermore indicating that encounter rates with prey may affect predation rates. In long-term laboratory experiments, A. nelsoni consumed more amphipods during low tide conditions than during high tide conditions. Many nemerteans in the field prefer particular environmental conditions (e.g. nocturnal low tides), which restricts the time available for successful feeding. In the long-term experiment, predation rates of A. nelsoni never exceeded 0.5 amphipods nemertean^–1 d^–1. Maximum feeding events were 3 or 4 amphipods nemertean^–1 d^–1, but this only occurred during 10 out of a possible 2634 occasions. Nemerteans that had consumed 3 or 4 amphipods during 1 day, consumed substantially less prey during the following days. Towards the end of the long-term experiment, average predation rates decreased to 0.2 amphipods nemertean^–1 d^–1, corresponding to predation rates reported for other nemertean species (0.1–0.3 prey items nemertean^–1 d^–1). We suggest that predation rates from laboratory experiments represent maximum estimates that may not be directly transferable to field populations. Additionally, low predator–prey encounter rates with preferred prey in the field may further limit the predation impact of nemertean predators in natural habitats.     

Behavioural evidence for a chemoreceptive function of the cerebral organs in Paranemertes peregrina coe (hoplonemertea: monostilifera)

The cerebral organs of nemerteans are complex neuroglandular structures whose function has never been clearly established. In this study, we have investigated the possibility that the cerebral organs in Paranemertes peregrina Coe might be chemoreceptors, by comparing prey detection and mucous trail- following ability in worms with and without cerebral organs. Removal of the cerebral organs abolished the recognition of prey trails but did not affect mucous trail-following. We conclude that a major function of the cerebral organs in Paranemertes is that of chemoreception for the detection of prey.     

Status of the Nemertea as predators in marine ecosystems

The ecology of nemertean predators in marine ecosystems is reviewed. Nemerteans occur in most marine environments although usually in low abundances. Some species, particularly in intertidal habitats, may reach locally high densities. During specific time periods appropriate for hunting, nemerteans roam about in search of prey. Upon receiving a stimulus (usually chemical cues), many nemertean species actively pursue their prey and follow them into their dwellings or in their tracks. Other species (many hoplonemerteans) adopt a sit-and-wait strategy, awaiting prey items in strategic locations. Nemerteans possess potent neurotoxins, killing even highly mobile prey species within a few seconds and within the activity range of its attacker. Most nemertean species prey on live marine invertebrates, but some also gather on recently dead organisms to feed on them. Heteronemerteans preferentially feed on polychaetes, while most hoplonemerteans prey on small crustaceans. The species examined to date show strong preferences for selected prey species, but will attack a variety of alternative prey organisms when deprived of their favourite species. Ontogenetic changes in prey selection appear to occur, but no further information about, e.g. size selection, is available. Feeding rates as revealed from short-term laboratory experiments range on the order of 1–5 prey items d^–1. These values apparently are overestimates, since long-term experiments report substantially lower values (0.05–0.3 prey items d^–1). Nemerteans have been reported to exert a strong impact on the population size of their prey organisms through their predation activity. Considering low predation rates, these effects may primarily be a result of indirect and additive interactions. We propose future investigations on these interactive effects in combination with other predators. Another main avenue of nemertean ecological research appears to be the examination of their role in highly structured habitats such as intertidal rocky shore and coral reef environments.     

Phylogeny and cladistic classification of terrestrial nemerteans: the genera Pantinonemertes Moore & Gibson and Geonemertes Semper

Evolutionary relationships among seven species from two genera ( Pantinonemertes and Geonemertes ) of terrestrial nemerteans (phylum Nemertea) were estimated by a Wagner analysis of 27 morphological, ecological and life history characters. Pantinonemertes was found to be a paraphyletic taxon, and it is suggested that this genus should be combined with Geonemertes to form a monophyletic group. A previous hypothesis for how terrestrial nemerteans evolved is discussed and compared to the results of the cladistic analysis. This suggests that terrestrial and semi-terrestrial species evolved from a marine ancestor; the upper littoral and marine environments have been recolonized by descendants from a terrestrial ancestor.     

Haemocyanin oxygen binding and the physiological ecology of a range of talitroidean amphipods (Crustacea) II. Effect of freezing,inorganic ions,and urate on O2 binding in vitro

Summary The effect of variations in [K], [Ca], [Mg], [NaCl], and [urate] on the in vitro O₂ binding properties of haemocyanin (Hc) from three talitroidean species, viz. the aquatic Apohyale pugettensis, the semi-terrestrial Megalorchestia californiana, and the semi-/euterrestrial Traskorchestia traskiana were studied. Freezing altered the cooperativity of Hc from A. pugettensis and M. californiana but not T. traskiana. Variations in [NaCl], [K], and [Mg] had no effect on cither O₂ affinity or cooperativity of the Hc except for A. pugettensis Hc where an increase in [Mg] resulted in an increase in both O₂ affinity and cooperativity. Increasing [Ca] or [urate] increased O₂ affinity of both A. pugettensis and M. californiana but not T. traskiana Hc. These effects were most marked in A. pugettensis. The results suggest a negative correlation between sensitivity to Hc effectors and the degree of terrestrial adaptation of a particular amphipod species.Abbreviations Hc haemocyanin - STR Stock traskorchestia ringer     

Ecological studies of the nemertean fauna in an estuarine system of the northwestern Gulf of Mexico

The distribution and abundance of nemerteans in the brackish-water lakes of Sea Rim State Park, Texas, near the Louisiana border, were studied and compared with other macrobenthos during one year. Six of 93 macrobenthic species collected were nemerteans (0.9% of the total number of specimens). Only one species of nemertean, Carinoma sp., was consistently present. This species is the most ubiquitous and, probably, the most abundant nemertean in the estuarine systems of the Texas coast. Carinoma sp. was collected at Sea Rim from a salinity range of 0–21 ppt and at other Texas estuaries from 2–26 ppt. Preliminary experiments with Carinoma sp. as predator and as prey indicated that it feeds on polychaete worms and in turn is fed upon by white (Penaeus setiferus) and brown (P. aztecus) shrimp.     

Preliminary survey of a nemertean crab egg predator,Carcinonemertes, on its host crab,Callinectes arcuatus (Decapoda,Portunidae) from Golfo de Nicoya,Pacific Costa Rica

The possible presence of egg predators in brood masses of portunid crabs from Pacific Central America has not been studied yet. This survey reports the finding of a nemertean crab egg predator on the portunid crab, Callinectes arcuatus, from the Golfo de Nicoya, Pacific Costa Rica. Nemerteans were found in the egg masses of 26 out of the 74 crabs for a prevalence of 35%. The intensity (mean number of worms/ infected crab) was estimated to be 18 with a variance of 1–123 worms/infected crab. No nemerteans were observed either in the 19 Callinectes arcuatus from Golfo Dulce (southern Pacific coast) and the 10 Portunus asper from Herradura-Jaco (central Pacific coast). This nemertean is a member of the genus Carcinonemertes, which has been reported from the Caribbean coast of Panama. However, the encountered Carcinonemertes sp. is the first published finding and report from Costa Rica and Pacific Central America.     

A new semi-terrestrial nemertean from California

A new species of semi-terrestrial monostiliferous hoplonemertean from California, Pantinonemertes californiensis sp. nov., is described and illustrated. The genus Pantinonemertes, transitional between marine and terrestrial habitats, provides evidence for one evolutionary line towards the colonization of land by nemerteans.     

Preliminary study of heat shock proteins in nemerteans

Nemerteans experience varying environmental temperatures during low tide exposures. Inducible heat shock proteins (hsps) have been reported for most organisms following both artificial heat stress and natural environmental temperature variations. This preliminary study reports the presence of hsps in the phylum Nemertea. A lethal temperature of 36 °C was determined for Paranemertes peregrina Coe, 1901. The nemerteans were exposed to a temperature of 34 °C for 2 h. After a 2 h recovery time, the worms were then analyzed for hsps by SDS–PAGE and western immunoblot protocols. Control worms were allowed to acclimate to ambient temperatures (13–15 °C) before hsp analysis. Hsp70 and hsp90 were detected in both the control and heat-shocked worms in highly variable concentrations, and the latter group had significantly elevated hsp70 levels. In addition, the analysis detected different isoforms of hsp70. The detection of hsps indicates a possible role in nemertean physiology during response to thermal stress, and potentially to other environmental challenges.     

THE EVOLUTION AND COMPARATIVE PHYSIOLOGY OF TERRESTRIAL AND FRESHWATER NEMERTEANS

(1) Parallel evolution from separate marine ancestors has given rise to two groups of genera of terrestrial nemerteans, representative of at least two different family stocks. They have colonized land by the direct route, moving up the shore on widely separated oceanic islands. The relationships between the known terrestrial and semi-terrestrial nemerteans, comprising seven genera and 15 species, are defined and their geographic distribution is discussed.
(2) In fresh water, three heteronemertean and nine hoplonemertean species are known. The hoplonemerteans arise from two different families representing two different evolutionary routes to fresh water, one by way of estuaries and the other via land. The distribution of freshwater nemerteans and the characters common to all species are discussed.
(3) Very little is known about the comparative physiology of land and freshwater nemerteans. However, information about the physiology of marine forms is combined with morphological differences from them found in terrestrial and freshwater species to suggest profitable lines of future research.
(4) Water relations pose a major problem for both terrestrial and freshwater nemerteans. The role of the cerebral organs, the blood and the excretory system in the osmotic physiology of some littoral nemerteans is beginning to be understood. These systems in land and freshwater forms have clearly distinctive features which need to be thoroughly investigated.
(5) Suggestions are given for valuable lines of investigation of the mucous glands, digestive physiology and general behaviour of terrestrial and freshwater nemerteans.     

Ecological implications of the reproductive biology of symbiotic nemerteans

A major problem for parasites is to ensure that offspring will reach a correct host. Responses to this problem include several reproductive adaptations. This review paper shows that Carcinonemertes has several such adaptations, including increased number of gonads and offspring, synchrony of hatching with host larval hatching, facultative parthenogenesis, and mating. Other nemerteans show different, but comparably adaptive, reproductive modifications for parasitism. In contrast, reproductive biology of the commensal Malacobdella resembles that of free-living nemerteans, being timed to coincide with plankton blooms that are food for settling young.It has been thought that nemerteans found in association with other animals usually have only causal relationships with those animals, and that actual parasitism is rare among nemerteans. However, it is being found that parasitism is both well developed and more common among nemerteans than was previously thought. Nemerteas show in their reproductive biology that they are adapted to the selective factors that are important in their ways of life, and we should be able to predict the life styles of these worms by knowing their reproductive ecology.     

Calcaneal features of the Greek Miocene primate Mesopithecus pentelicus (Cercopithecoidea: Colobinae)

This paper investigates substrate preferences of the Greek Colobine Mesopithecus pentelicus WAGNER, from the Miocene of Pikermi, by examining selected functional features of the calcaneus that distinguish between arboreal and terrestrial Cercopithecidae. Mesopithecus possesses a relatively long proximal calcaneal region associated with a slightly low and wide surface for the insertion of m. triceps surae. These features approximate that of semi-terrestrial Cercopithecidae and would suggest terrestrial cursorial activities. On the other hand, the relatively long and narrow proximal calcaneo-astragalar facet, similar to that of most arboreal species, would provide ampler subtalar movements. The mosaic of these features implies a semi-terrestrial way of life and conforms to the savanna-woodland paleoenvironment of Pikermi, Greece. These features appear to be well associated with foot function and change of habitus and are used to examine scenarios of the evolutionary history of the Colobinae.     

Prothonotary warbler nestling growth and condition in response to variation in aquatic and terrestrial prey availability

Aquatic prey subsidies entering terrestrial habitats are well documented, but little is known about the degree to which these resources provide fitness benefits to riparian consumers. Riparian species take advantage of seasonal pulses of both terrestrial and aquatic prey, although aquatic resources are often overlooked in studies of how diet influences the reproductive ecology of these organisms. Ideally, the timing of resource pulses should occur at the time of highest reproductive demand. This study investigates the availability of aquatic (mayfly) and terrestrial (caterpillar) prey resources as well as the nestling diet of the prothonotary warbler (Protonotaria citrea) at two sites along the lower James River in Virginia during the 2014 breeding season. We found large differences in availability of prey items between the two sites, with one having significantly higher mayfly availability. Nestling diet was generally reflective of prey availability, and nestlings had faster mean growth rates at the site with higher aquatic prey availability. Terrestrial prey were fed more readily at the site with lower aquatic prey availability, and at this site, nestlings fed mayflies had higher mean growth rates than nestlings fed only terrestrial prey. Our results suggest that aquatic subsidies are an important resource for nestling birds and are crucial to understanding the breeding ecology of riparian species.     

Patterns of abundance variation in reef fishes near an artificial reef at Guam

Synopsis Development of the fish community on a submerged 16 m barge and variation in fish abundance on nearby transects were surveyed twice monthly for twenty months. A steady increase in abundance was observed for certain fishes on the barge, whereas a few species exhibited distinct seasonal variation on both the barge and transects. Most of the seasonal species settled between March and May.Some seasonal species appeared to be site selective in their settlement and consequently settled juveniles were clumped in their distribution. An abundance of preferred topographical features may be why settlement was relatively high at the study site and indirectly why predators became significantly (r₃ = 7.67^***, N = 37) more abundant at the study area during the months of maximum prey settlement. Concurrent settlement of several species during the same few months may be important because juveniles become an abundant food source to predators during those few months only. Periodic swamping of predators by abundant juvenile prey may improve the chances for individuals of rarer prey species to be overlooked and therefore be succesfully recruited.     

Forest succession and prey availability influence the strength and scale of terrestrial‐aquatic linkages in a headwater salamander system

1. Trophic linkages between terrestrial and aquatic ecosystems are common and sensitive to disruption. However, there is little information on what causes variation in the strength and spatial scale of these linkages. 2. In the highly aquatic adults of the headwater salamander Gyrinophilus porphyriticus (family Plethodontidae), use of terrestrial prey decreases along a gradient from early‐ to late‐successional riparian forests. To understand the cause of this relationship, we tested the predictions that (i) terrestrial prey abundance is lower in late‐successional forests, and (ii) G. porphyriticus adults cannot move as far from the stream to forage in late‐successional forests, thus limiting access to terrestrial prey. 3. We established 100‐m long study reaches on six headwater streams in the Hubbard Brook Experimental Forest, New Hampshire. Three reaches were in early‐successional forests and three were in late‐successional forests. We conducted pitfall trapping for invertebrate prey in June and July of 2005, with three traps at 0, 2, 5 and 10 m from the stream at each reach. In June, July and August of 2004 and 2005, nighttime salamander surveys were conducted at each reach along ten, 10‐m long by 2.5‐m wide transects perpendicular to the stream. 4. Abundance of terrestrial prey was consistently lower in late‐successional forests, suggesting that consumption of terrestrial prey by G. porphyriticus is affected by prey abundance. Contrary to our prediction, G. porphyriticus adults moved farther from the stream in late‐successional forests, suggesting that habitat conditions in late‐successional forests do not limit movement away from the stream, and that lower abundances of terrestrial prey in these forests may cause salamanders to move farther from streams. 5. Our results provide novel insight on the extent of terrestrial habitat use by G. porphyriticus. More broadly, these results indicate that major habitat gradients, such as forest succession, can affect the strength and scale of terrestrial‐aquatic linkages. Application of this insight to the design of vegetation buffers along headwater streams would have widespread benefits to freshwater ecosystems.     

Created pools and food availability for fishes in a restored salt marsh

Trophic support functions for fishes are a key goal of salt marsh restoration. Food availability in restored sites may be enhanced by creation of shallow pools, which are important sources of prey items in tidal wetlands. Young restored salt marshes are typically sparsely vegetated and are subject to rapidly changing geomorphology. Scouring and sedimentation create and fill shallow depressions, producing a shifting mosaic of tidal pools. In a large (8-ha) southern California experimental restoration site, we created shallow pools and assessed their development of foods for fishes. Created pools quickly developed abundant invertebrate prey, with densities exceeding those found in older, naturally formed pools (P < 0.0001). Opportunistic mobile and disturbance-associated taxa (calanoid copepods, nematodes, Polydora complex, and Trichocorixa reticulata) accounted for higher invertebrate densities in created pools. We repeated experiments in spring, summer, and fall and found seasonal variability in trophic development. We also applied bottom-up (nitrogen addition) and top-down (fish exclusion) treatments to pools. Some measures of algal biomass were increased by nitrogen fertilization (P = 0.001–0.06), but there were no upward-cascading effects on invertebrate composition or abundance. Fish abundance in the site varied seasonally, but there were no compelling effects of fish exclusion treatments on algal or invertebrate abundance. Incorporating shallow depressions into salt marsh restoration projects is a potential tool to jumpstart fish-support functions.     

Distribution of cichlid fishes in the littoral of Lake Bacalar, Yucatan Peninsula

The distribution of cichlids in Lake Bacalar was assessed from January to September 1996, in eight shallow-water (< 2 m) stations, using a 20 m long seine net. Temperature, salinity/conductivity and dissolved oxygen were sensor-obtained; depth, submerged vegetation and bottom type were determined by visual inspection. Affinities between stations, based on fish abundance and environmental parameters, were analyzed by multivariate methods. Littoral of Bacalar town was the site with highest richness, diversity and abundance, probably promoted by the additional urban waste of organic matter. PCA defined two station-groups, one associated with muddy substrates, the other one with rocky/sandy bottoms. Cichlids are more abundant over muddy bottoms with abundant submerged vegetation, probably because of the abundance of prey and shelter.