Food dependent movement of periwinkles (Littorina littorea) associated with feeding fronts.
Animal populations (Observations)
Scheibling, Robert E.
|Publication:||Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2009 National Shellfisheries Association, Inc. ISSN: 0730-8000|
|Issue:||Date: August, 2009 Source Volume: 28 Source Issue: 3|
|Geographic:||Geographic Scope: Canada Geographic Code: 1CANA Canada|
ABSTRACT Consumer aggregations have the potential to drastically
change the distribution and availability of resources. One form of
aggregation observed in marine benthic invertebrates is the feeding
front: a dense band of consumers that travels in a directional manner
through a food patch, leaving a cleared area behind it. By artificially
creating spatial heterogeneity in the distribution of a filamentous
green alga, the formation of a feeding front of periwinkles Littorina
littorea was induced on a rocky intertidal shore. The position of the
front, the density of snails that comprised it, and the movement of
individual snails in and around the front were monitored over a period
of 14 days. During that period, the front advanced at an average speed
of 2.25 cm d l and the density of snails in the front varied between 10
and 24 snails 100 [cm.sup.-2]. Temporal variation in snail density was
negatively correlated with wave action. Snails on the trailing edge of
the front or on bare rock behind the front exhibited directional
movement towards the front, but snails in the front moved shorter
distances than those on bare rock. These results support previous
findings of resource-dependent movement as a causal mechanism of front
formation in marine benthic habitats.
KEY WORDS: Littorina littorea, feeding front, snail, intertidal, movement, aggregation
Striking patterns in the spatial distribution of predators or grazers can arise when a resource is consumed in a structured manner (Sole & Bascompte 2006). A linear feeding aggregation, or "front," is one such pattern that has been observed in a wide range of taxa, including bacteria (Keller & Segel 1971), insect larvae (Burrows & Balciunas 1997), ungulates (Gueron & Levin 1993), marine snails (Silliman et al. 2005), sea stars (Ormond et al. 1973, Scheibling 1980, Scheibling & Lauzon-Guay 2007), and sea urchins (Breen & Mann 1976). Although feeding fronts can vary in size and form, they generally share some common features: a dense band of consumers advancing through a region of high food availability; low densities of consumers ahead of and behind the front; and a sharp gradient in food availability at the front.
Feeding fronts, when they destructively consume a resource, can have dramatic effects on ecosystems. For example, fronts of littorinid snails have been linked to the disappearance of salt marshes in the United States (Silliman et al. 2005) and sea urchin fronts are widely known to decimate kelp forests and seagrass beds, causing decreases in habitat complexity, productivity, and biodiversity (e.g., Johnson & Mann 1988, Rose et al. 1999). The aggregate effect of many simultaneously feeding individuals greatly accelerates the depletion of food resources. Sea urchins, for example, must exceed a threshold density to effectively feed on large kelps (Breen & Mann 1976, Scheibling et al. 1999, Lauzon-Guay & Scheibling 2007a). Furthermore, concentrated grazing pressure can alter feeding preferences (Wright et al. 2005) and prevent the regeneration or recovery of prey populations.
The ubiquitous nature of feeding fronts suggests that simple behavioral mechanisms may be responsible for their formation. Silliman et al. (2005) proposed that chemotaxis (change in the direction of movement in response to a chemical stimulus) leads to formation of feeding fronts of snails (Littoraria irrorata) in salt marshes. However, other studies indicate that resource-dependent dispersal can provide a more parsimonious explanation for front formation (Wilson & Richards 2000, Lauzon-Guay et al. 2008). Empirical evidence that animals commonly adjust their movement in response to local resource densities (Sutherland et al. 2002) is consistent with this explanation. For example, freshwater snails have been shown to spend more time in patches of periphyton than on patches without food (Kawata & Hiroko 1999). Elucidating the role of abiotic and biotic factors in regulating individual movement and, in turn, the distribution of consumers is essential for understanding the process of aggregation and the dynamics of front advance (Lauzon-Guay et al. 2008, Lauzon-Guay et al. 2009, Snider & Gilliam 2008).
The common periwinkle Littorina littorea is ubiquitous on rocky shores in the North Atlantic where it plays an important functional role in structuring algal assemblages of the intertidal and shallow subtidal zones (Lubchenco 1978, Petraitis 1983, Petraitis 1987, Chapman 1989, Scheibling et al. 2009). By grazing ephemeral filamentous algae, periwinkles facilitate colonization of larger fleshy macroalgae, such as fucoids and Chondrus crispus (Lubchenco 1980, Lubchenco 1983, Scheibling et al. 2009). Intense grazing pressure by L. littorea can also directly preclude the growth of fucoids (Vadas 1992). Dense fronts of L. littorea have been observed consuming filamentous green algae on rocky shores along the Atlantic coast of Nova Scotia, and there is anecdotal evidence of similar fronts in southern England (Warner 2001). However, the mechanisms of front formation in marine snails, and the dynamics of these feeding fronts, have not been documented.
To test the hypothesis the snail feeding fronts arise through resource-dependent dispersal when resources are patchily distributed, we experimentally induced a grazing front of Littorina littorea on a rocky intertidal shore. We monitored the movement of the front, and of individual snails in and around the front, in relation to the size and distribution of a food resource (filamentous green algae), the density of snails, and wave action (which affects foraging ability). We compare our findings to empirical and theoretical studies of front dynamics in other consumers.
MATERIAL AND METHODS
Measures of significant wave height (SWH, mean of the largest one third of waves measured) were obtained from a meteorological buoy (www.meds-sdmm.dfo-mpo.gc.ca) located at the mouth of Halifax Harbour (Buoy ID C44258, 44[degrees]34'N, 63[degrees]30'W). The buoy is located 13 km from the study site, and wave conditions at a nearby site (within 1.5 km) correlate well with those recorded by the buoy (Lauzon-Guay & Scheibling 2007b). Our experiment was conducted along a section of shore that is partially protected from direct impact of waves by a rock outcrop.
Experimental Manipulation and Measurements
Dense fronts of Littorina littorea were observed advancing onshore at this site in June 1987 (R. E. Scheibling, personal observation), consuming a film of ephemeral green algae that colonized the intertidal zone after a major ice scour event had denuded the shore in March (Minchinton et al. 1997). To recreate this situation, we simulated an ice--scouring event by clearing a 2-m wide swath through the intertidal zone in May 2006. All erect macroalgae and sessile invertebrates were scraped from the rock, which was then intensively burned using a propane torch to destroy residual algal crusts and holdfasts. By the next spring (April 2007), a thick mat of filamentous green algae (Enteromorpha intestinalis) had formed in the mid zone of our experimental area, below a narrow band of juvenile Fucus vesiculosus that had colonized in the high zone (Fig. 1). Littorina littorea occurred at low density in the low zone, which remained devoid of macroalgae or sessile invertebrates. On April 12, 2007, approximately 150 L. littorea were collected from an adjacent intertidal boulder field and added to the low zone of the experimental area. Over the next two weeks, a front of L. littorea formed at the lower margin of the patch of E. intestinalis in the mid zone (Fig. 1).
[FIGURE 1 OMITTED]
To track the movement of individual snails in the experimental area, 20 haphazardly selected L. littorea were tagged in each of 4 locations: (1) the leading edge of the front (snails in the half of the front closest to the Enteromorpha mat), (2) the trailing edge of the front, (3) the "bare" rock (without macroalgae) behind the front, and (4) the Fucus zone above the mat. Snails were tagged on site during low tide on May 10, 2007 by affixing a 2.5-mm diameter, numbered plastic bee-tag to the upper part of the shell with small glob of marine epoxy. The snails were not removed from the substratum during tagging, minimizing disturbance associated with the procedure, which lasted only a few seconds. The epoxy with the embedded tag was smoothed along the shell surface, minimizing any effect of the tag on snail movement.
Positions of tagged snails were recorded daily at low tide for 2 wk (May 10-23). A series of eyebolts (affixed to the bedrock with marine epoxy) served as benchmarks: 5 eyebolts were positioned at 2545 cm intervals along a line parallel to the shore in the high zone above the Enteromorpha mat, and two were positioned 85 cm apart on bare rock in the low zone, on April 29 (Fig. 1). The experimental area and 3 m along the shore on either side of it were thoroughly searched for tagged snails. The position of each tagged snail was triangulated on site by measuring the distance from the snail to two furthest eyebolts above the algal mar (120 cm apart), using a plastic measuring tape (1-mm accuracy).
A digital photograph of the experimental area (including the benchmarks) was taken on April 29 and then daily from May 10 to 23 (Fig. 1). The images were scaled using the "imtransform" function in Matlab (The MathWorks Inc), with the eyebolts serving as a spatial reference system. This enabled us to obtain comparable measurements directly from the series of photographs. The position of the front (relative to the eyebolts) was measured from these photographs at 25 equally spaced points along the edge of the front (the edge is defined as the boundary between the Enteromorpha mat and the snail aggregation). Snail density in the front, on the Enteromorpha mat in advance of the front, and on bare rock behind the front, was measured by randomly positioning 5, 10 x 10 cm quadrats in each location in the images. Density was not measured in the Fucus patch because the thalli obscured the snails, rendering counts unreliable. We also recorded the location of the tagged snails from these images (relative to benchmarks) as: (1) leading or (2) trailing edge of the front, (3) Enteromorpha mat, (4) Fucus patch, or (5) bare rock in the low zone.
To estimate the grazing rate of the littorinid front in terms of biomass of Enteromorpha intestinalis consumed, two replicate 5 x 5 cm samples from the center of the mat (not grazed by snails) were collected on May 11 and 13, 2007. These were dried for 24 h at 60[degrees]C and weighed (0.001 g accuracy) to obtain dry weight. The weight of algae per unit area was then used to estimate grazing rate of the front from daily rate of advance of the front. The daily grazing rate of snails was calculated as the linear advance of the front over one day divided by the density of snails in the front.
To examine potential tagging effects and tag loss, 10 Littorina littorea were tagged in the laboratory using the same procedure as in the field. The snails were maintained in an aquarium with flowing seawater for the duration of the field experiment. We observed no mortality or morbidity, unusual behavior (relative to untagged snails maintained in other aquaria), or tag loss during that period.
Density of snails in the front, in the Enteromorpha mat, and on bare rock were compared using 2-way analysis of variance (ANOVA) with location (fixed, 3 levels) and date (fixed, 13 levels) and their interaction. Snail counts were square-root transformed to meet the assumptions of normality and homoscedasticity. Multiple comparisons between habitats were done using Tukey HSD test (Zar 1999).
Daily displacement of snails from the leading or trailing edge of the front, the Fucus patch, and the area of bare rock were compared using 1-way ANOVA with location (fixed, 4 levels). Distance data were log-transformed to meet the assumptions of normality and homoscedasticity. Nonuniformity of the distribution of movement direction was assessed separately for each day and habitat using Rayleigh test (Zar 1999).
By the start of our tagging experiment on 10 May, the leading edge of the front of Littorina littorea had advanced 24 cm in an onshore direction from its position on April 29 (when benchmarks were erected). It then advanced another 27 cm during the experiment (May 10-22), indicating a relatively constant rate of advance over both intervals: 2.20 and 2.25 cm [d.sup.-1], respectively (Fig. 2A). Between April 29 and May 18, 5,000 [cm.sup.2] of the Enteromorpha mat was grazed by the front, completely clearing the algae from the experimental area (Fig. 2A). There was a strong negative correlation between the average advance of the front and the remaining area of E. intestinalis (Pearson r = -0.97, P < 0.001). The biomass of E. intestinalis did not differ significantly between measurement dates (t-test, P = 0.474), and data were pooled to give an average biomass of 0.03 ([+ or -] 0.01 SD) g [cm.sup.-2]. Thus, we estimated the rate of grazing of E. intestinalis by the littorinid front as 0.06 g [(cm of front).sup.-1] [d.sup.-1.]
During the experiment, the average density of Littorina littorea in the front declined from about 24-10 snails 100 [cm.sup.-2] (Fig. 2B). Snail density was much lower within the Enteromorpha mat (1-6 snails 100 [cm.sup.-2]), and few snails occurred on bare rock behind the front (<1 snail 100 [cm.sup.-2]) (Fig. 2B). ANOVA indicated an interactive effect of sampling date and location on the density of snails during the experiment ([F.sub.22,146] = 3.15, P < 0.001). Density was greater (Tukey test, P < 0.05) in the front than in the Enteromorpha mat or on bare rock at all sampling dates, and greater in the Enteromorpha mat than on bare rock on 4 of 8 days (May 15, 16, 18, and 19; Fig. 2B). Snail density in the front and in the Enteromorpha mat varied significantly (P < 0.05) over time. Although all measurements were taken around low tide, we also observed the front by snorkeling during high tide on May 14 and 15, 2007. There were no apparent differences in the density of snails in the front, or in their spatial distribution among locations, between tidal states.
[FIGURE 2 OMITTED]
Much of the temporal variation in density of Littorina littorea in the front was explained by variation in significant wave height (SWH) during the 24-h period prior to sampling ([r.sup.2] = 0.57; [t.sub.10] = -3.93, P = 0.003). Fewer snails were found in the front during periods of high waves than during calm periods (Fig. 3A). The rate of advance of the front also tended to decrease with SWH, although the relationship was not statistically significant ([r.sup.2] = 0.24; [t.sub.10] = -2.04, P = 0.071; Fig. 3B). The relationship between the rate of advance of the front and the density of snails in the front also was nonsignificant ([r.sup.2] = 0.14; [t.sub.10] = 1.64, P = 0.134; Fig. 3C).
[FIGURE 3 OMITTED]
The proportions of snails that were tagged in the front or in other locations (Fucus patch, bare rock) at the start of the experiment and found in the front on subsequent days, rapidly converged over time (Fig. 4). On the first day after tagging, 67%, 62%, 53%, and 32% of snails, initially tagged in the leading and trailing edges of the front, Fucus patch, and on bare rock respectively, were found in the front. Whereas snails moved in and out of the front during the experiment, the proportion of tagged snails initially in the front (leading and trailing edges) that remained in the front progressively decreased as the Enteromorpha mat was consumed, and front began to disperse by May 17. Snails originally on bare rock increased in number until May 15 (47% in the front), whereas those on the Fucus patch were most abundant in the front on May 11 (52%).
On the first day of sampling, tagged Littorina littorea on bare rock moved a greater distance (mean [+ or -] SE: 121.3 [+ or -] 12.1 cm) than snails in the front (leading edge: 30.3 [+ or -] 8.7 cm, trailing edge: 45.2 [+ or -] 7.6 cm) or Fucus patch (60.0 [+ or -] 16.5 cm) ([F.sub.3,56] = 9.07, P < 0.001). On subsequent sampling dates, there were no significant differences in the average distance moved by snails among locations; however, the power of these tests was limited by small sample sizes. We did not detect a significant relationship between the distance moved by individual snails and SWH in any location ([r.sup.2] < 0.1, P > 0.2). Snails at the leading edge of the front generally moved in a down-shore direction away from the front, with significant departures from random movement (Raleigh test, P < 0.05) on 4 dates (May 11, 12, 17, and 18; Fig. 5). Conversely, snails on bare rock generally moved up-shore towards the front (significant on May 11, 12, 14, 15), and those at the trailing edge of the front generally moved up-shore towards the leading edge (significant on May 12 and 14). Snails in Fucus patch above the Enteromorpha patch generally moved down-shore towards the Enteromorpha patch (significant on May 11, 18, and 21).
[FIGURE 4 OMITTED]
Snails have highly-developed neurosensory systems, and their capacity to follow gradients (e.g., slope, humidity, food, predators) is well documented (Bingham 1972, Chapman 2000, Rochette & Dill 2000, Wollerman et al. 2003). In our study, Littorina littorea located along the trailing edge of the front or on bare rock behind the front exhibited directional movement towards the front. However, the time-scale of our observations (24 h) does not allow us to resolve whether the snails followed environmental cues (e.g., chemical stimuli from algae or conspecifics, slope of the shore) or simply encountered the mat of Enteromorpha intestinalis through random movement. The propensity of snails to follow mucus trails of conspecifics (Erlandsson & Kostylev 1995) also may have influenced their movement pattern and ability to locate the feeding front. Once in contact with the algal mat, snails in the front tended to move less than those on bare rock behind the front, at least while the mat was extensive, suggesting that L. littorea reduces its movement in the presence of food. Food-dependent dispersal also has been observed for freshwater snails (Kawata & Hiroko 1999), and incorporating this behavior significantly improves the fit of dispersal models (Snider & Gilliam 2008). Littorina littorea in the front tended to move greater distances on average, and their movement was more variable, once the algal mat was almost completely consumed (May 18-19), suggesting that some of the snails moved away from the front once the food source was depleted.
[FIGURE 5 OMITTED]
Whereas Littorina littorea on bare rock and at the trailing edge of the front showed directed movement toward the front, snails at the leading edge of the front (i.e., those in direct contact with macroscopic food) showed directed movement away from the front (towards bare rock). The fact that snails at the leading edge of the front moved away from the front, suggests that snails are unlikely to remain in the front for extended periods of time. Over the first day of our experiment, 33% of snails left the front, and after a week only 20% of snails originally tagged in the front remained there, it is unlikely that we overlooked tagged snails, particularly in the front. Tags were easily detected and the study area was searched thoroughly. The movement of snails away from the front suggests that heat stress (Soto & Bozinovic 1998, Jones & Boulding 1999) and increased risks of dislodgement (Alfaro & Carpenter 1999) and predation (Catesby & McKillup 1998) associated with openly foraging in the upper intertidal zone, outweigh the benefits of readily available food, once a level of satiety is attained. The importance of satiety on snail behavior is further supported by the difference in movement direction between snails at the leading and trailing edge of the front. A threshold level of satiety, at which snails retreat to safer locations, is likely to vary with the intertidal location of the front and the level of risk to individuals.
A cohesive front of Littorina littorea advanced through the area colonized by Enteromorpha intestinalis until the algal mat was entirely consumed. There was a positive trend (although not statistically significant) between the rate of advance of the front and snail density in the front, consistent with previous observations of sea star and sea urchin fronts (Scheibling 1980, Lauzon-Guay & Scheibling 2007a). There was a negative relationship between the rate of advance of the front and the area of the algal mat, suggesting that the front moved more rapidly once the food resource was depleted. Conversely, increases in food after high tides can reduce the downward migration of Littoraria scabra in mangroves (Alfaro 2007). Abiotic factors, such as wave action, also affect the movement and sheltering behavior of littorinid snails (Pardo & Johnson 2006). The density of L. littorea in the front was negatively correlated with significant wave height and the rate of advance of the front generally decreased with significant wave height, although the relationship was not statistically significant. Similarly, wave action affects feeding fronts of sea urchins by reducing the density of urchins and the rate of advance of the front (Lauzon-Guay & Scheibling 2007a, 2007b).
Our findings support the hypothesis that resource-dependent dispersal, combined with spatial heterogeneity in food distribution, are sufficient conditions for the formation of feeding fronts (Lauzon-Guay et al. 2008). By artificially creating a patch of a filamentous green alga, we induced the formation of a feeding front of Littorina littorea, and observed differences in the movement behavior of individual snails within and outside of the front that were consistent with food-dependent dispersal. Thus, we predict that these snails, when abundant, will form feeding fronts when the distribution of their algal food resources is discontinuous or patchy. Similar fronts of L. littorea have been observed at an intertidal site in the Bay of Fundy, Nova Scotia, with snail densities (23-55 snails 100 [cm.sup.-2]; R. E. Scheibling, unpublished data) comparable to those in our experimental front. Our manipulation simulated a major disturbance event, such as an ice-scouring ora severe storm, which promotes the establishment of early successional algal forms that are highly susceptible to littorinid grazing (McCook & Chapman 1997). Variations in environmental factors (e.g., aerial exposure, temperature, wave action) across the intertidal gradient, influence patterns of algal distribution and abundance, as does the spatial distribution of grazers in this zone. Thus, the seasonal migration of littorinid snails, from low to high intertidal zones in the spring (Warner 2001), also could generate spatial heterogeneity in algal distributions, leading to the formation of feeding fronts.
The authors thank John Lindley, Terra McMullen, Jenn Jones, and Devin Lyons for their help in the field. The authors also thank the National Research Council of Canada's Aquaculture Research Station in Sandy Cove for granting access to the field site. The research was funded by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada (NSERC) to RES. JSLG was supported by a graduate scholarship and a postdoctoral fellowship from NSERC.
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JEAN-SEBASTIEN LAUZON-GUAY (1,2) * AND ROBERT E. SCHEIBLING (1)
(1) Department of Biology, Dalhousie University, Halifax, Nova Scotia B3H 4J1 Canada; (2) Fisheries and Oceans Canada, Institut Maurice-Lamontagne, 850 route de la Mer, Mont-Joli, Quebec, G5H 3Z4, Canada
* Corresponding author. E-mail: email@example.com
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