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Feeding rates of the nemertean Prosorhochmus americanus (Hoplonemertea) on two species of gammaridean amphipods
Article first published online: 28 SEP 2010
© 2010, The American Microscopical Society, Inc.
Volume 130, Issue 1, pages 34–42, March 2011
How to Cite
Caplins, S. A. and Turbeville, J. M. (2011), Feeding rates of the nemertean Prosorhochmus americanus (Hoplonemertea) on two species of gammaridean amphipods. Invertebrate Biology, 130: 34–42. doi: 10.1111/j.1744-7410.2010.00211.x
- Issue published online: 18 FEB 2011
- Article first published online: 28 SEP 2010
- Jassa falcata;
- Corophium cf. insidiosum
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.
Nemerteans are able to exert a significant effect on the densities of their prey; however, measuring feeding rates for these animals that can be readily applied to the field has proven difficult (Ambrose 1991; Thiel et al. 2001). Many of the early measurements of feeding rates were obtained through short-term investigations that highlighted the ability of nemerteans to take advantage of prey items offered ad libitum, but did not follow the rate of predation after they had reached satiation (e.g., McDermott 1976, 1988). Feeding rates obtained over longer periods of time indicate that while the rates of predation for these animals are highly variable, they are likely to be lower than previously thought (McDermott 1993; Thiel & Kruse 2001; Thiel et al. 2001). Rates of predation for preferred prey have been estimated for relatively few nemerteans, even though this is one of the first steps in understanding the role nemerteans play in community structuring (McDermott 1984, 1993; McDermott & Roe 1985; Thiel et al. 2001).
Prosorhochmus americanusGibson et al. 1986 is a hermaphroditic, viviparous hoplonemertean found under cemented valves of the oyster Crassostrea virginica Gmelin 1791 or among the byssal threads of mussels (Brachidontes exustus Morris 1975, or Mytilus edulis Linnaeus 1758) in the intertidal zone on rock jetties and pilings in Florida, North Carolina, South Carolina, and Virginia (Gibson et al. 1986; Maslakova & Norenburg 2008; Turbeville & Caplins 2010). Neither prey preference nor predatory behavior has been described for this nemertean, which can be an abundant member of the fouling community (pers. obs.), where it might have significant effects on prey populations. The objectives of this investigation were to determine (1) the feeding rate of P. americanus on members of two species of suspension feeding gammaridean amphipods, Jassa falcata Montagu 1808 and Corophium cf. insidiosum Crawford 1937, and (2) whether the predation rate varied between light and dark conditions. This investigation supplements the small number of long-term feeding studies on nemertean predators and their prey, and provides a necessary starting point towards understanding the role that members of P. americanus play in the structuring of fouling communities.
All nemerteans and prey items were collected between August and December 2009 from the north jetty of Rudee Inlet in Virginia Beach, Virginia (36°49′49″N, 75°58′06″W). Individuals of Prosorhochmus americanus were collected by prying stunted oysters (Crassostrea virginica), blue mussels (Mytilus edulis), and associated material from the surface of the rocks (see Turbeville & Caplins 2010). The material was transported to the lab in sealable plastic bags and then transferred to large glass culture dishes, where the worms would crawl to the sides and subsequently be removed.
Amphipods used in feeding-rate trials were collected by scraping the sediment and associated epifauna from the surface of the rocks. They were maintained in aquaria with artificial seawater (30‰) for the duration of the investigation, and fed a mixture of rotifers (Brachionus plicatilis Muller 1786) and powdered algae (Ulva sp.), loosely following the feeding protocol of Nair & Anger (1979). The tanks were kept at room temperature (average=24°C) with constant aeration, and water changes (25% of the total volume) were performed daily. The amphipod Jassa falcata was identified using the key provided by Conlan (1990); all other amphipods were identified using the key of Bousfield (1973).
Estimation of feeding rates
Preliminary feeding trials were performed with four individuals of P. americanus per glass Pyrex dish (20.3 × 15.2 × 5 cm). Worms were offered the isopod Sphaeroma quadridentatum Say 1818 (3–4 per dish, n=6 replicates), and the gammarid amphipods Hyale plumulosa Stimpson 1857, C. cf. insidiosum, J. falcata, and Stenothoe minuta Holmes 1903 (4 per dish, n=1 replicate per species). Potential prey species were offered to the worms separately over a 2-d period, and in combination (3 of each amphipod and 2 isopods) over an additional 2 days (n=3 replicates). Dishes were examined for predation after 24 h. The number of prey items offered and the number consumed were recorded.
The feeding rate experiments were conducted from October to December 2009. To measure feeding rates, a single sexually mature individual of P. americanus was placed in a Pyrex dish with five individuals of the amphipods J. falcata (n=10 replicates) or C. cf. insidiosum (n=14 replicates). Mature worms were distinguished from immature individuals by the presence of gonads or developing juveniles, which can be clearly seen through the body wall (Fig. 1). Amphipods were selected with no consideration to their sex; however, an attempt was made to select adult individuals of approximately the same size across all replicates. A control dish was maintained for each species of amphipod to monitor the rate of mortality. The dishes were filled with 150 mL of natural seawater, 50 mL of rotifer culture, and a very small amount of freeze-dried, powdered algae (Ulva sp., suspended in artificial seawater before use). This volume of water was maintained at all times, thereby simulating high-tide conditions. A cleaned oyster shell fragment was placed in each dish as a refuge for the worms and amphipods (see Thiel et al. 2001). Additional rotifers and Ulva sp. powder were added to the dishes as needed. Water changes were performed every 3 d, whereby 50% of the total volume (100 mL) was removed and replaced with 75 mL natural seawater and 25 mL rotifer culture. All animals were kept at room temperature (21–26°C) for the duration of the investigation.
A 7-day acclimation period was established to allow the nemerteans to acclimate to laboratory conditions, i.e., ambient temperature and light regime. If a nemertean failed to consume a single prey item or died during this 7-d period, the nemertean along with any data collected were excluded from the study. If a nemertean consumed a prey item and continued to live past this period, all predation events recorded for the nemertean were used in the feeding-rate calculations, including those from the first 7 d. The dishes were checked for signs of predation twice daily around 08:00 and 17:00 hours, at which times the lights were turned on and off, respectively. It is important to note that total darkness was not achieved when the lights were out. Dead amphipods were removed and examined with a dissecting microscope to determine whether they had been consumed by the worms or had died of other causes. In order to maintain a constant prey density, all dead or consumed amphipods were replaced with healthy individuals. Predation events were recorded according to whether they occurred under light or dark conditions.
An amphipod consumed by a nemertean could be distinguished from one that had died of other causes (i.e., damage inflicted by conspecifics, or other unknown causes) by a lack of tissue in the exoskeleton, with tissue occasionally remaining in the antennae and other extremities, along with the presence of the intestinal tract, which often remained following the evacuation of the surrounding tissue (see McDermott 1984:fig. 3B for images of evacuated exoskeletons). Additionally, the exoskeleton of a consumed amphipod could be readily distinguished from a freshly molted exuvia. Exuviae typically exhibited a dorsal break or split in the cuticle, often right behind the last segment of the head, accompanied by a longitudinal split occurring laterally between the plates of the coxae and the peraeon, while in a consumed amphipod, the exoskeleton was generally left intact along the dorsal and lateral surface, and may or may not have had discernable damage ventrally. The natural light coloration (a mottled orange/yellow) and semi-translucent body of the nemertean allowed an obvious color change to be observed following predation, as the gut diverticula became filled with the dark pigments of the amphipod, causing the worm to appear dark brown or even black (Fig. 1) for 3–4 d. This change in coloration also allowed us to attribute predation events to recently emerged juveniles of P. americanus, in the few instances that the juveniles were able to feed before being detected and subsequently removed from the dish. The predation events for juvenile worms were not used in calculating the feeding rates, even though in some instances it was unclear if the amphipod was killed and consumed solely by the juvenile or killed by the adult worm and then consumed by both adult and juvenile. The emergence of juvenile worms was recorded throughout the feeding rate experiment.
During the course of the investigation several nemerteans crawled too far from the water surface and succumbed to desiccation. Dead worms were immediately replaced with healthy worms that had been recently collected from the field and kept in the lab without exposure to prey items. A total of four (of 24) experimental nemerteans were replaced throughout the feeding rate experiment: three replacements for the dishes containing C. cf. insidiosum as prey item (n=36, 11, and 21 d after the start of the experiment), and one for a dish containing J. falcata as prey item (n=21 d after the start of the experiment). Feeding rates were calculated for individual nemerteans, and a new rate was calculated for each nemertean that was replaced. The feeding time (# days) for the four replacement worms and their predecessors differed from that of the other individuals in the study (Fig. 3).
The length and width of each nemertean was recorded before and after the study period. All measurements were made on unrelaxed worms while they were actively gliding. Twice-daily counts of predation events were collected for nemerteans with the prey items J. falcata (n=54 d of data collection) and C. cf. insidiosum (n=44 d of data collection). All consumed amphipods were preserved in alcohol and later imaged with a digital camera (Panasonic Lumix DMC-FX37, Panasonic Corporation of North America, Secaucus, NJ, USA) mounted on a Nikon SMZ 1000 dissecting microscope (Nikon Corporation, Tokyo, Japan). Imaged amphipods were measured from the tip of the rostrum to the end of the telson using Image J software (National Institute of Mental Health, Bethesda, MD, USA, available at http://rsbweb.nih.gov/ij/; Abràmoff et al. 2004). Measurements of all amphipods offered to the worms were not made.
Student's t-test was used to compare rates of predation between nemerteans exposed to the two prey species (J. falcata and C. cf. insidiosum). To provide an approximately equivalent comparison, only data collected during the first 40 d of the study period were used for nemerteans with J. falcata, due to the occurrence of a “fasting” event on the part of several of the nemerteans (see “Results”). Data obtained over the entire 44-d period were used for nemerteans with C. cf. insidiosum. Regression analyses were performed to determine if there was a relationship between (1) nemertean body size and the number of prey items consumed, and (2) the average feeding rate and the number of days data were collected for each nemertean.
A χ2 analysis was performed on the number of predation events relative to the photoperiod (α=0.05, df=1, critical value=3.841). The expected values were calculated by assuming that there would be an even distribution of predation events between light and dark conditions. As the nemerteans and their prey were exposed to an average of 10 h of light and 14 h of dark, we assumed that 40% of predation events would occur during the day (when the lights were on in the lab) and 60% at night (when the lights were off). An α value of 0.05 was used to determine the statistical significance of all tests performed.
Prey items consumed
In our initial feeding trials, individuals of Prosorhochmus americanus were found to consume members of three different species of amphipod (# consumed/# offered: Jassa falcata [7/13], Corophium cf. insidiosum [5/13], Stenothoe minuta [3/13]), as well as the isopod Sphaeroma quadridentatum (1/25). The worms did not consume individuals of the amphipod Hyale plumulosa (0/4) during these initial trials.
The nemerteans exposed to the prey item J. falcata had an average (±standard deviation [SD]) feeding rate of 0.19±0.14 amphipods nemertean−1 d−1, as calculated over the first 40 d of the study period (Fig. 2A). An average feeding rate of 0.26±0.13 amphipods nemertean−1 d−1 was calculated for worms with C. cf. insidiosum feeding over variable time periods (most 30 d or longer: Fig. 2B). The difference between these two feeding rates was not statistically significant (two-tailed t-test, p=0.098). A nemertean never consumed more than two amphipods between the two daily checks. The maximum number of amphipods consumed over 24 h was three, and one individual consumed six amphipods over a 48-h period. Such a high level of predation (>2 amphipods nemertean−1 d−1) was only seen on six separate occasions for three out of 24 worms, one with J. falcata as the prey item, and two with C. cf. insidiosum. A drop in feeding rates following these high levels of predation was not observed, with typically only 1 or 2 d passing before the worms fed again. These three nemerteans maintained higher rates of predation than any of the other worms for the duration of our investigation (0.53, 0.42, and 0.39 amphipods nemertean−1 d−1, n=40, 33, and 44 d, respectively; Fig. 3). The feeding rates as calculated for individual nemerteans were highly variable, with the lowest feeding at a rate of only 0.05 amphipods nemertean−1 d−1 and the highest at 0.53 amphipods nemertean−1 d−1 (n=21 and 40 d, respectively; Fig. 3A).
Factors affecting predation rates
While carrying out the feeding rate experiment, a disruption in the feeding of the nemerteans presented with J. falcata occurred, whereby all feeding came to a stop roughly 40 d into the experiment and did not continue again for 9 d (Fig. 2A). During this period, two of the nemerteans that had been feeding at a relatively high rate (those responsible for most of the recorded predation events, consuming 0.53 and 0.35 amphipods nemertean−1 d−1) now contained numerous large juveniles. Feeding rates for these individuals resumed at a normal level following the emergence of a relatively large number of juveniles (i.e., six and four, respective to above-mentioned feeding rates). Juveniles emerged on the same day towards the end of the 9-d period. These worms produced a total of 16 juveniles each during the experiment (Fig. 3A). However, a consistent correlation between feeding rates and number of juveniles produced was not seen. The feeding rates for the other nemerteans presented with J. falcata were much lower (<0.18 amphipods nemertean−1 d−1), and it was not uncommon for a period of 7 d or more to lapse between predation events for these worms, although these predation pauses appeared to be unrelated to juvenile development. A similar feeding disruption was not observed for nemerteans feeding on C. cf. insidiosum, and fewer juveniles emerged from these worms throughout the study (Fig. 3B). A total of 66 juveniles emerged from the worms with J. falcata, and 38 from those with C. cf. insidiosum. With exception of the two worms mentioned above, juvenile worms appeared in the dishes somewhat sporadically, usually one or two at a time, with an average of 11 d passing between emergence events (calculated for all adult worms).
Regression analyses provided no support for an association between worm size and number of prey items consumed. An R2 value of 0.034 was obtained for worms with J. falcata (n=10), and 0.055 for worms with C. cf. insidiosum (n=14). Additionally, no support was obtained for a relationship between the individual feeding rate and the number of days feeding data were collected (R2=0.0028 for worms with C. cf. insidiosum, and 0.1363 for worms with J. falcata).
The average (±SD) length, at the start and completion of the study, of nemerteans with J. falcata was 11.2±2.8 mm, and 11.4±2.5 mm, respectively. For nemerteans with C. cf. insidiosum, the starting average length was 7.7±4.4 mm and the final average length was 9.8±2.2 mm. The average length, from rostrum to telson, of amphipods consumed by the nemerteans was found to be 4.7±0.9 mm for J. falcata and 2.6±0.5 mm for C. cf. insidiosum.
Predation in relation to photoperiod
There was no statistically significant difference in predation between dark or light periods with C. cf. insidiosum as a prey item. However, we found a significant difference in the amount of predation occurring during light or dark periods for worms that were offered J. falcata, with considerably more predation occurring when it was dark (p=0.0033; Table 1).
|Corophium cf. insidiosum|
The average feeding rate of individuals of Prosorhochmus americanus estimated in this study (0.19–0.26 amphipods nemertean−1 d−1) lies within the range of average feeding rates measured for other hoplonemerteans under similar experimental conditions (McDermott 1993; Roe 1993; Thiel et al. 2001). The rates for this study were estimated with amphipod prey items offered ad libitum, and the movement of the prey was restricted to the confines of the dish, thus greatly limiting their ability to escape from the nemerteans. These conditions are not present in nature; therefore, these rates probably represent an upper limit of prey consumption for these nemerteans (see also Thiel et al. 2001). This view is supported by the fact that during our investigation no nemertean consumed all of the prey items offered in a single day, suggesting that satiation was reached after consuming three or fewer amphipods.
The feeding rates we estimated for P. americanus are congruent with those obtained by Thiel et al. (2001) for the rocky-shore hoplonemertean Prosorhochmus nelsoni Sánchez 1973 (average ∼0.20 amphipods nemertean−1 d−1, maximum=0.50 amphipods nemertean−1 d−1), even though there were potentially significant differences in experimental design between the two investigations, namely dish size and water coverage. For our investigation, nemerteans and prey were placed in large glass Pyrex dishes (20.3 × 15.2 × 5 cm). In contrast, Thiel et al. (2001) used small Petri dishes (8.8 × 1.4 cm). The difference in total volume between these dishes is ∼1.5 L. The usable volume of the Pyrex dish is 3.6 times greater than that of the small Petri dish, with usable volume defined as the space in the dish occupied by water (water height=1 cm) and therefore accessible to the nemerteans and their prey. We suggest that the similarity in feeding rates despite differences in dish size has indirect implications for estimating the potential foraging distance of a hungry nemertean, an issue which has previously been addressed only for soft-bottom intertidal nemerteans (Roe 1976; Thiel 1998; Kruse & Buhs 2000).
The decision was made to estimate feeding rates while simulating high tide, due to the practical concern of maintaining enough water in a low-tide simulation sufficient to prevent desiccation of the worms and their prey. However, Thiel et al. (2001) found that individuals of P. nelsoni consumed more amphipod prey during simulated low tide versus simulated high tide, suggesting that low tide provides an advantage to successful predation. Considering that we recorded similar rates of feeding without simulating low tide, it is clear that being submerged did not prevent predation by these nemerteans in the laboratory. It is important to note that while we were simulating high tide by maintaining a constant volume of water, we did not attempt to simulate the wave action and strong currents that are also present during high tide at the rock jetty. This investigation and others have revealed that intertidal hoplonemerteans are capable of capturing and consuming prey while covered by water (Kruse & Buhs 2000; Thiel et al. 2001); however, field observations suggest this does not often occur under natural conditions (Roe 1976; Kruse & Buhs 2000). It may be that nemerteans are more effective at capturing prey at low tide, when their chemoreception is enhanced and the chance of their prey escaping is limited (Roe 1970, 1976; McDermott 1976; Thiel & Reise 1993; Thiel 1998; Kruse & Buhs 2000). Wave action and strong currents are additional constraints to successful predation by intertidal hoplonemerteans, which are unable to maintain contact with their prey organism following the initial capture, and face the threat of being swept away in the current themselves (McDermott 1976; Kruse & Buhs 2000; Thiel et al. 2001).
We suspect that P. americanus is active during night or crepuscular low tides, as has been documented for other intertidal nemerteans (Roe 1970, 1976; Thiel 1998; Thiel et al. 2001; Wang et al. 2008). It is noteworthy that most individuals of P. americanus directly observed in the field at low tide during daylight hours were inactive, typically lying motionless under oysters. They also exhibited negative phototaxis in the laboratory (pers. obs.). This activity pattern presents several advantages for the nemertean, namely, decreased risk of desiccation, less competition from visual predators, and a potential reduction in the ability of prey to escape, assuming visual cues are the basis of avoidance (Roe 1970, 1976; McDermott 1976; Thiel 1998; Thiel et al. 2001).
Consistent with observations of higher activity during the night for other nemerteans (Roe 1970, 1976; Thiel 1998), we found significantly higher predation on the amphipod Jassa falcata in dark conditions (p<0.05). Light has been shown to inhibit the activity of nemerteans, and Wang et al. (2008) found that photoperiod had a significant effect on predation rates of the palaeonemertean Procephalothrix simulus Iwata 1952, with predation reduced when worms were exposed to 24 h of light.
On the rock jetty both J. falcata and Corophium cf. insidiosum typically reside in mud tubes (see Ulrich et al. 1995; pers. obs.). However, under laboratory conditions, individuals of C. cf. insidiosum constructed tubes much more often than J. falcata. During the feeding rate observations, small pieces of dried sea lettuce (Ulva sp.) provided as food for the amphipods were found incorporated into the tubes of C. cf. insidiosum. In the absence of Ulva fragments or other material, the amphipods constructed tubes with only their mucosal secretions. Tubes of J. falcata were only rarely seen in the Pyrex dishes during the experiment, and this species is known to be more selective in choosing tube-building materials than the amphipod C. insidiosum (Ulrich et al. 1995). The tube provides the amphipod with protection from visual predators (Nelson 1979); however, it may also provide a fixed location where the amphipod can be easily detected by a predator relying on chemoreception (see Bartsch 1973; McDermott 1984, 1988, 1998 for predation studies on tubicolous amphipods). Laboratory experiments have exposed the subtleties of nemertean chemosensory systems in prey detection, and revealed that chemical cues play a major role in prey detection (Amerongen & Chia 1982; Kruse & Buhs 2000). It is possible that by inhabiting tubes, C. cf. insidiosum was more vulnerable to predation irrespective of light or dark conditions, especially if, as is likely, the nemerteans were relying on chemoreception to locate their prey. This may account for the somewhat higher daytime consumption of C. cf. insidiosum relative to J. falcata (Table 1).
An additional factor potentially affecting prey consumption in viviparous nemerteans is the extent of juvenile development. We observed that a 9-d “fasting” period in at least two of the nemerteans exposed to the amphipod J. falcata may have been correlated with the presence of large juveniles within these worms. These two worms exhibited relatively high rates of predation preceding the fasting period, feeding at rates >0.23 amphipods nemertean−1 d−1. Such high rates of feeding may have accelerated juvenile development, and as the juveniles increased in size, this may have limited the movement of the adult nemertean, making it less efficient at capturing prey. The large juveniles also compress the intestine of the adults (pers. obs.), perhaps having a negative effect on food intake. Juveniles measured within 24 h of emergence from adults (by anal parturition) averaged 3.7±0.55 mm in length (n=36 individuals). Development is not synchronous, and juveniles of all stages are found in a single worm (Gibson et al. 1986; pers. obs.). This lack of synchronicity complicates predictions regarding the impact juvenile development may have on prey consumption. The number of juveniles and their developmental stages appears to be highly variable in each worm, and may explain why a potential correlation between a high feeding rate and large number of juveniles, leading to a break in feeding pattern, was seen in only two out of 24 worms.
During the preliminary feeding trials, individuals of P. americanus were observed to feed on members of three species of amphipod (C. cf. insidiosum, J. falcata, and Stenothoe minuta) and on one occasion captured and consumed the isopod Sphaeroma quadridentatum. However, after the conclusion of the experiments reported herein, we discovered that the nemertean also would prey on the amphipod Hyale plumulosa if given sufficient time. Members of three of these amphipod species are common on the jetty (J. falcata, C. cf. insidiosum, and H. plumulosa). At low tides during daylight hours, aggregates of inactive P. americanus are often found in close proximity to individuals of H. plumulosa, which prefers regions of the substratum lacking sediment, whereas, with a few exceptions, the tube-dwelling amphipods are situated in sediment-laden areas of the rocks closer to the rock/bottom interface, well below where most nemerteans are found. We observed that individuals of P. americanus will consume members of H. plumulosa regularly under laboratory conditions (i.e., high-tide simulation, constant prey density), but at a much lower rate than measured for J. falcata and C. cf. insidiosum (0.069 amphipods nemertean−1 d−1, n=13, feeding over a 31-d period) (unpubl. data). Adults of H. plumulosa are large and fast moving, and are likely able to evade nemertean predation by swimming through the water column, doing so more easily than either adults of J. falcata or C. cf. insidiosum (pers. obs.), which likely rely on their mud tubes for protection. It may be that these amphipods are captured by the nemerteans exclusively during low-tide conditions. However, our field observations revealed that individuals of H. plumulosa are capable of crawling very quickly and will even jump when out of water, behaviors that may make them difficult for a nemertean to capture even at low tide. The size differences that exist between these three species of amphipod may also influence predation rates. The consumed individuals of H. plumulosa averaged a length of 7.96 mm, nearly twice that of J. falcata (4.7 mm) and three times that of C. cf. insidiosum (2.6 mm). While such large individuals of H. plumulosa may be more difficult for a nemertean to capture, once consumed, the worm is likely to remain satiated for a longer period of time, resulting in a lower feeding rate.
Our results are consistent with previously published studies of other suctorial hoplonemerteans (e.g., McDermott 1988, 1993; Thiel & Kruse 2001; Thiel et al. 2001). Populations of P. americanus may have the potential to affect community structure by altering the distribution and abundance of their prey species. However, we agree with Thiel et al. (2001; see also McDermott 1988) that feeding rates in the laboratory may not reflect those in the field, as in the field prey encounters are likely limited (because the time window for foraging is restricted to nocturnal low tides), foraging distances may be longer because of disjunct predator–prey distribution, and prey may be able to emigrate from regions of high nemertean activity. Therefore, the extension of laboratory feeding rates to natural communities for estimating the impact of nemertean predation on prey abundance may be misleading (see Thiel et al. 2001). We advocate field investigations of predation as the next critical step to evaluate the impact of these predators on community structure, and our single observation of P. americanus attacking and feeding on an amphipod (H. plumulosa) at low tide before sunrise suggests that such studies should be feasible.
The relationship between feeding rates and juvenile development remains unclear and merits further study. Reproduction has been mentioned as an intrinsic factor possibly affecting predation rates in nemerteans (Kruse & Buhs 2000; Thiel et al. 2001), but to date has not been investigated thoroughly. The study of reproduction in P. americanus represents a unique challenge in that juveniles develop without synchronicity and reproduction occurs year round. Future research focusing on the relationship between feeding and reproduction in both viviparous and oviparous nemerteans will enhance our understanding of an additional factor potentially affecting predation rates and provide a more detailed view of how predator–prey interactions contribute to community structuring.
The number of different prey species that were consumed in the lab suggests that this nemertean is possibly an opportunistic predator of gammaridean amphipods, but further study is warranted (see McDermott 1998 for a summary of amphipod species known to be nemertean prey). Quantitative field sampling will be necessary to establish the relative abundance of amphipod species in the field, but our preliminary observations suggest that members of C. cf. insidiosum, H. plumulosa, and J. falcata are present in large numbers, although the tube-dwelling species and the nontubicolous H. plumulosa inhabit separate zones. We have rarely observed individuals of P. americanus near these tubicolous-amphipod zones during daytime low tides; rather, most occurred within the Hyale zone. Although we have one observation of an individual of P. americanus consuming an individual of H. plumulosa in the field, whether this nemertean consumes this amphipod more frequently than the other two under natural conditions remains an open question pending field investigations.
Acknowledgments. We thank Dr. James Vonesh for help with experimental design and advice on statistical analyses. We are grateful to Dr. Martin Thiel and an anonymous reviewer for providing helpful comments which have improved the quality of this manuscript. We also thank Danielle Marie Donner for help in the estimation of predation rates on H. plumulosa.
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