removal of fungal and total organic matter from decaying cordgrasseaves by shredder snails

J. Exp. Mar. Biol. Ecol., 171 (1993) 39-49

0 1993 Elsevier Science Publishers B.V. All rights reserved 0022-0981/93/$06.00

39

JEMBE 02000

Removal of fungal and total organic matter from decaying cordgrass leaves by shredder snails

Steven Y. Newell a and Felix B grlocher b

“Marine Institute, University of Georgia, Sapelo Isiund, Georgia, USA; ‘Biology Depurtment, Mount Allison

University, Sackville. Net+’ Brunswick. Canadu

(Received 22 December 1992; revision received 23 March 1993; accepted 2 April 1993)

Abstract: Several lines of evidence from the literature have pointed to the saltmarsh periwinkle (Lictoruriu

irrorata [Say]) as a potentially important shredder of standing, decaying cordgrass (Spartina alterniflora

Lois&) shoots. Periwinkles prefer to ingest dead-shoot material and possess enzymes capable of lysis of cordgrass plant-structural and fungal-wall polymers. We offered natural, standing-dead leaf blades to periwinkles in an attempt to determine the rates at which the snails would rasp away and ingest material of the

decaying-shoot system, and whether the snails would selectively remove living-fungal mass (measured as ergosterol) from the system. The larger snails tested (14 mm shell height) took 42”‘, of the total organic mass of the blades during 6 days of exposure, and exhibited selectivity for fungal-occupied portions of blades by

removing 69% of the living-fungal organic mass. Based on observed removal rates, about 2-3:, ‘day ’ of

the organic mass of standing-dead leaf blades could be lost to snail grazing in marsh areas where the snails are most densely concentrated (> 400 individuals m ml of shell length > 5 mm). In a preliminary comparison

of adjacent marsh areas of equivalent canopy height, the one without periwinkles had a 4 x greater standing crop of dead lcaves. Periwinkles are likely to be important controlling agents of fungal standing crops

and important shapers of fungal community dynamics in cordgrass marshes, in that the standing, decaying substratum for fungal growth and the potential for fungal spccics successions are radically changed by the

snails’ activities.

Key words: Ergosterol; Fungi; Invertebrate shredder; Littoraria irrorutu: Saltmarsh; Spartina crltern$oru

INTRODUCTION

Saltmarsh periwinkles (the prosobranch gastropod Littoraria irrorata [Say]; syn-

onym Littorina irrorata Say; see Reid, 1989) are among the most common invertebrates

of smooth-cordgrass (Spartina afternzjlora Loisel.) saltmarshes (Daiber, 1982). In

south-temperate North American marshes, periwinkles can occur at densities of over

100. me2 (e.g., Stiven & Hunter, 1976; West & Williams, 1986; Vaughn & Fisher,

1988; Newell, 1993a). Such common marsh animals must have considerable impact

upon the marsh ecosystem through their feeding activities (see, e.g. Stiven & Kuenzler,

1979; Cammen et al., 1980; Norton et al., 1990).

Studies of saltmarsh-periwinkle feeding activities have yielded inconsistent results.

Marples (1966) characterized the periwinkles as sediment feeders (as opposed to

Correspondence address: S.Y. Newell, Marine Institute, University of Georgia, Sapelo Island, GA 31327, USA.

40 S.Y.NEWELLANDF.BARLOCHER

green-shoot feeders), based on uptake of 32P from spray-labelled sediment (as opposed

to injection-labelled shoots). However, Marples (1966) pointed out that the 32P spray-

ing contacted shoot material externally; it could have thusly labelled standing-dead

leaves in addition to sediment. The spraying may also have labelled snails (their

radioactivity was measured as whole animals) via activity of the cyanobacterial lichen

(Arthropyreniu halodvtes [Nyl.] Am.) that grows within shells of L. irroruta (see Kohlm-

eyer & Volkmann-Kohlmeyer, 1991). Odum & Smalley (1959) had earlier stated that

“Spurtinn detritus [composed] at least a part of the food of the snail”, and Alexander

(1979) Stiven & Kuenzler (1979) and Kemp et al. (1990) obtained evidence that dead

shoots of smooth cordgrass were a major portion of the diet of L. irrorutu. Bertness

(1984) found that a north-temperate zone littorinid (Littorinu littoreu L.) would also

ingest shoot material of S. altern$oru. Alexander (1979) suggested that plant particles ingested by L. irrorutu might not be

digested (based on appearance of plant pieces in feces), but Barlocher et al. (1989a,b)

found that L. irrorutu was enzymatically capable of lysis of both cordgrass structural

molecules and ofwall components of Spurtinu-decomposer fungi. Bebout (1988) showed

that assimilation efficiencies for L. irrorutu ingesting mycelia of two species of Spurtinu ascomycetes were near 50 “i;, , and Barlocher & Newell (1993) found digestive efficiency

(acid-insoluble-ash method) by L. irrorutu for standing, decaying Spurtinu leaves to be

517;. We conducted the present experiment to determine rates at which saltmarsh

periwinkles of two size classes could withdraw organic and fungal mass from naturally

decaying cordgrass leaves offered to them as potential food.

METHODS

A summary of our experimental procedures is given in Table I. Saltmarsh periwinkles

(L. irrorutu) of two size classes (near 5 and 14-mm shell length [ = “height” of Reid

TABLE I

Abridged flow chart for experimental procedures.

(1) Collect standing, decaying cordgrass leaves from marsh areas lacking large snails

(2) Halve leaf pieces lengthwise

(4) Arrange three types of incubations: 20-ml jars, 6 days: 60-ml jars, 3 days; 60-ml jars, 6 days

(5) Set up each type of incubation with and without snails” (5-mm snails in 20-ml jars; 14-mm

snails in 60-ml jars)

(3) Assign each corresponding set of halves: one half to jar incubations; the twin half to imme- diatc analysis

(6) Measure organic mass and ergosterol content for leaf pieces: prior to incubation; after incubation with snails; after incubation without snails h

a Replication: n = 3. ’ Pool leaf pieces within replicate jars for analysis

SNAIL SHREDDING OF CORDGRASS 41

(1989), meaning length of coiling axis], measurement after Bingham [ 19721) were collected from shoots of smooth cordgrass (S. altev@ora) in marshes of Sapelo Island (Pomeroy & Wiegert, 1981) in September, 1992. Larger snails were taken from outer surfaces of standing leaves or stems (there were no snails present on the sediment surface), and smaller snails from the curled, inside (adaxial) surfaces of standing-dead leaf blades near the ligule, where they were hidden (see Smalley, 1959). Larger snails were taken from a marsh area with sediment elevation 240 cm above mean low water springs, an average cordgrass-shoot density of 127.4 ( + 20.4 SD, n = 3 replicate 0.25-m’ censuses) per m’, an approximate mean shoot height of 40 cm, and an average density of snails of 459.6 (_t 35.2) per m’. Smaller snails were taken from a nearby marsh area (about 10 m distant) that contained only small snails hidden in curled, dead leaves (sediment elevation, 227 cm; approximate mean shoot height, 45 cm).

Snails were placed in loosely capped 60-m] (large snails, 5 I jar-‘) or 20-ml (small snails, 10. jar -‘) screw-cap (teflon lining in cap) glass jars containing 2 ml (large jars) or 0.5 ml (small jars) of seawater (20%,). Six replicate jars were prepared for large snails and three for small snails, and an equal number of jars without snails was prepared. Jars received natural, filtered sunlight in the laboratory (ranges of daylight [measured at 1400 h] and temperature [measured at 0900 and 14001: 15 to 975 PE’ me2 1 s -’ photosynthetically available radiation [median, 3751; 21 to 32 “C [median, 23 o I).

Standing-dead leaf blades offered to snails were collected from the same area of marsh where our smaller group of snails had been collected. Blades collected were the 1st or 2nd below the current yellow-green (senescent) leaf on a shoot (i.e. the dead leaves on a shoot that had most recently changed from yellow-green to brown: see Newell, 1993a). Adherent clay was rinsed away (Newell et al., 1992) and a 5-cm length was cut from each leaf between 5 and 10 cm distal to the ligule. Because high variability was anticipated for microbial content of the leaves (see Table 2 of Newell et al., 1988), we used a leaf-halving technique (Fell et al., 1984). The 5-cm lengths were folded in half and split lengthwise with a scalpel. The two halves were photocopied for area recording (Newell et al., 1989), and one half was allotted to a pre-exposure set, the other to exposure in the jars ~~ith~without snails. Four halves were placed upright in each jar such that contact among leaves was minimized.

Some of the leaves used in this experiment contained distinctly blackened, irregu- larly shaped patches. Direct-microscopic observation revealed that the blackened patches were occupied by the ascomycete fungus Bwrgenerula spartinae Kohlm. & Gessner within areas occupied by the commonly predominant species Phaeosphaeria spartinida Leuchtmann (see Kohlmeyer & Gessner, 1976; Newell, 1993a). Because B. ~pa~tina~ may contain high levels of ergosterol per unit fungal mass (Newell et al., 1987), we sampled blackened patches to determine if these were likely to add to ergosterol variability among experimental jars. Four standing-dead leaves containing large blackened areas (46% of total area) were cut into their blackened and lighter portions, and

42 S.Y.NEWELLAND F.BARLOCHER

areas of these portions were recorded. Ergosterol analysis of the separate portions was

conducted as described below.

Jars were incubated for 3 days (large snails and corresponding no-snail jars only)

or 6 days (all other jars). The seawater in each jar containing snaiIs was exchanged

for fresh seawater daily, and the seawater from the snail-free jars was replaced with

the old seawater from the snail jars, so that leaves in snail-free jars would experience

contact with snail excreta.

After incubation, snails were removed from jars and released after measurement of

shell lengths (vernier calipers for large and dissecting microscope for small snails).

Leaves were removed and snail fecal material was rinsed from them. Average shell

length per jar for small snails ranged from 4.8 to 5.3 mm (corresponding to 1.5 to

2.0 mg dry body mass, after Smalley [ 19591); the range for large snails was 13.1 to

14.7 mm (24.8 to 34.7 mg). Thus, total snail dry body mass (shell length per jar times

mass per unit shell length) + cm -* leaf area was similar among jars within a range of

x 10 to 15 mg*cm-‘.

Analytical procedures for pre- and post-exposure leaf halves were identical. Each

5-cm length was cut latitudinally into two parts: one l-cm piece for organic-mass

measurement; one 3-cm piece for ergosterol (an index molecule for membranc-

containing eumycotic fungal mass: Newell, 1992). The bottommost 1 cm was dis-

carded. Pieces from each replicate jar were pooled as a single analytical replicate.

Organic-mass measurement followed Newell et al. (1991) and liquid-chromatographic

assay of ergosterol was after Newell (1993b), with chromatographic conditions as

described by Newell et al. (1988). Organic-mass and ergosterol contents of

post-exposure leaf-halves were compared to contents of corresponding pre-exposure

halves to find effects of incubation with~without snails. Note that if snail grazing

stimulates fungal productivity (see Ingham, 1992), our estimates of rates of ergosterol

removal would be conservative.

Statistical procedures used {analysis of variance [ANOVA] with SNK [Student-

Newman-Keuls] least-significant-range testing) were those of the SPSSjPC + 4.0 sys-

tem (NoruSis, 1990). Angular transformation (Sokal & Rohlf, 1981) was used with

percentage and ratio data.

RESULTS

There were no statistically significant (p < 0.05) differences for organic or ergosterol

densities (mass - cm -’ abaxial leaf area), or ergosterol concentrations (pg. g -’ organic

mass), among treatment sets for halves of leaves that were not incubated in jars

(pre-exposure sets). Average pre-exposure organic density was 9.3 mg. cm-’ ( 2 0.8,

1 SD; range, 7.2 to 10.4 per replicate). Average ergosterol density was 8.6 c(g + cm-’

(+ 1.6; range, 6.7 to 10.4); average ergosterol concentration was 934 pg .g-’ organic

mass (k 170; range, 718 to 1323). Density of ergosterol for blackened leaf areas


(occupied by B. spartinae) was 16.0 ( t 0.1) pg. cm -* abaxial leaf area and for lighter

areas (occupied by P. spartinicolu) 10.5 ( & 1.9) pg. cm-*.

Without snails, there was no detectable (~~0.05) decrease in organic or in ergos-

terol density for leaves in any of the three types of incubation (small jars, 6 days; large

jars, 3 or 6 days) (Fig. 1). There was statistically significant (p<O.O5) interaction be-

tween type of incubation and presence/absence of snails in the extent to which both

organic (p< 0.03) and ergosterol (p< 0.02) densities were reduced by snail grazing

(Fig. 1). Grazing by large snails for 6 days reduced organic density by 42x, signifi-

cantly (~~0.05) more than 3-day grazing by large or 6-day grazing by small snails

(23-25%). A similar pattern was observed for ergosterol (Fig. l), but the percent re-

ductions for ergosterol (36-69%) were greater than those for organic mass. However,

when the ratios between percent remaining organic mass and ergosterol were tested,

significance level for 2-way interaction between type of incubation and presence/absence

of snails was ~~0.08, and only the ratio for 6-day large snails (1.9) was significantly

(p < 0.05) different from the other two snail-grazing ratios (1.3-1.4).

-

L

0- 0+ E- E+ 0- 0+ E- Ei- 0- 0+ E- E+

ORGANIC MASS (0), ERGOSTEROL (E), & SNAILS (+ OR -)

Fig. 1. Effects of incubation of leaves of Spartim alternl~orora with and without exposure to saltmarsh periwinkles (Litkwaria irrorata), as percentages of original densities (mass cm -’ leaf) of organic mass and ergosterol. Leftmost group of bars, small (5-mm shell length) snails, exposure for 6 days; center group, large (14 mm) snails, 3 days; rightmost group, large snails, 6 days. Significant 2-way interaction (ANOVA, ~~0.03) was detected between type of incubation and presence/absence of snails for both variables. Error

bars show 1 SD (n = 3 replicate incubations).

44 S.Y. NEWELL AND F. BARLOCHER

Large snails removed organic mass from leaves at statistically equivalent rates during 3- and 6-day incubations (60-67 pg * rng-’ dry body mass * day-r) (Fig. 2). Small snails removed less (p = 0.05): an average of 27 pg. mg-’ . day-‘. Large snails at 3 days removed ergosterol at a more rapid rate than small snails during 6-day incubations (106 versus 3.5 ng . mg-’ dry body mass 9 day -‘) (p = 0.03) but the rates for the two incubation periods for large snails (82- 106 ng . mg - ’ . day-‘) were not significantly different (SNK, p>O.O5; Fig. 2).

Direct observations under the dissecting microscope revealed that snails had concentrated their radular scraping on the abaxial surfaces of leaves, removing portions of the former mesophyll chlorenchyma and its overlying epidermis and leaving relatively more material of the longitudinally oriented vascular bundles (especially the major vascular bundles as opposed to the minor bundles; see Anderson, 1974). Ascomata (sexual reproductive structures) of the two species of ascomycetes observed in the experimental leaves (P~laeosp~ue~ff spariinic~l~ and B~er~e~e~~a spar~i~~e~ were lodged in the former mesophyll chlorenchyma with openings (ostioles) through the abaxial epidermis centered above adaxial furrows, and were often partially eaten or completely removed. There was no obvious discrimination against either fungal species; the distinctly blackened (melanized) areas in which B. spartinae produced ascomata were not apparently undergrazed. Large snails grazing for 6 days removed most visible fungal material, and enough of the former mesophyll chlorenchyma that leaves were reduced to bundles of shreds (see Fig. 2 of Newell et al., 1989).

0 E 0 E 0 E

ORGANIC MASS (0) & ERGOSTEROL (E)

Fig. 2. Mean ( + 1 SD, n = 3) rates (day-‘) of removal of organic mass (1(g) and ergosterol (ng) from leaves of Spurtinn ulterniJora per mg dry body mass of snails (Littoraria irroratn). Groups of bars as in Fig. 1 (left, small snails, 6 days; center, large, 3 days; right, large, 6 days). ANOVA for organic mass, p = 0.05; for

ergosterol, p = 0.03.


DISCUSSION

Bebout (1988) discovered that at least 70% of fecal pellets produced by L. irrorutu

that had fed in smooth-cordgrass marshes contained fungal remains. Our results

confirm his conclusion that saltmarsh periwinkles feed on fungi from decaying

leaves of S. alterm~oru, and they bolster Alexander’s (1979) and Bailocher &

Newell’s (1993) findings, respectively, that: (a)periwinkles regularly ingest dead tissue

of smooth-cordgrass shoots; and (b) periwinkles can grow on food consisting of

standing-dead leaves of S. altern$oru naturally containing fungal mass or (at lower

rates) on pure mycelium of Spartina fungi. When our larger periwinkles were allowed

to feed on leaves for 6 days, they selectively removed fungal mass (at almost twice

the rate for removal of total organic mass; Fig. 1). That this removal was accompa-

nied by ingestion was evidenced by the fact that fecal pellets were produced in

the jars, not suspensions of shredded leaf bits. Using a rough conversion factor

(200 mg fungal organic mass per mg ergosterol; this is not well established, and

may be high due to the presence of B. spartinae in some of our leaves: see Results,

and Newell [ 19921; Gessner & Chauvet [ 1993]), one can calculate that living-fungal

organic mass constituted about 25-30% of the ingesta of snails in our experimental

jars.

Three explanations (not mutually exclusive) of the selective fungal ingestion might

be: (1) both snails and fungi compete for the same types of plant tissue; (2) snails are

attracted to densely fungal-occupied tissues; and (3) fungal digestion of plant tissues

softens them to the extent that snail rasping is more effective at removing material.

Bebout (1988) found that saltmarsh periwinkles did not prefer mixtures of fungal

mycelium (including P. spartinicolu [as Phaeosphaeria typharum]) and dead cordgrass

shoots over the shoot material alone. This may mean that the dead material already

contains enough fungal material to maximize snail attraction (as Bebout proposed), or

that snail attraction to densely fungal-occupied areas is caused by chemical alteration

of the area that reduces its repulsiveness (due to phenolic antifeedants: Valiela et al.,

1984; Norton et al., 1990; Newell, 1993a) and/or structural toughness (Norton et al.,

1990; Bergbauer & Newell, 1992). In any case, selective ingestion of fungal-altered

areas would result in optimization of amino-acid assimilation, based on Barlocher

et al.‘s (1989b) data for periwinkle-gut enzymatic releases from fungal-occupied Spartina

material.

We recognize that our experimental conditions could exaggerate the extent to which

periwinkles would naturally remove material from decaying cordgrass, since cordgrass

leaves were offered without surface sediment as an alternative food source. However,

in separate experiments (Barlocher & Newell, 1993) we offered L. irroruta natural

surface sediments versus naturally decayed cordgrass leaves (each food exchanged for

fresh material every 4-5 days) in 60-ml jars as in the present experiment. The peri-

winkles appeared to avoid contact with the sediment (see Vaughn & Fisher, 1992) and

did not grow (loss of 1.5 mg organic mass per snail [about IO-mm shell length] over


2 months, equivalent to starved controls), whereas dead leaves permitted a gain of 1.3 mg per snail (cf. Stiven & Hunter, 1976).

Our smaller snails removed total and fungal organic mass from leaves at a slower rate, per unit snail body mass, than did the larger snails (Fig. 2). This is contrary to what might be expected, since rate of periwinkle growth decreases with increase in snail size (Stiven & Hunter, 1976). The smaller snails may have spent unnaturally long periods in hiding in our jars, or smalier snails may not be as well equipped to tear away material of decaying leaves, and depend more on ingestion of clay-film deposits scraped from leaves (see Newell et al., 1992). Note, however, that when organic removal per unit snail organic mass is calculated ~~c~~~~~g organic mass of the shell (Barlocher & Newell, 1993), the ratio between rates for small and larger snails is reduced by 15 “/b .

Our larger snails were actually small relative to the maximum size attained in the marsh by saltmarsh periwinkles (e.g. 24 mm shell length: West & Williams, 1986), and rates of removal of total organic mass and ergosteroi for truly large snails are unknown, so we can use our removal rates for 14-mm snails only preliminarily and speculatively to calculate potential impacts of snail grazing on the marsh. Number of snails per unit leaf area in our large experimental jars was ~0.4 cm-2. Shoots in the area of marsh where our larger snails were collected bore an average of 1.0 ( i 0.7, n = 10) dead and unshredded standing leaves, and average number of visible snails per dead-leaf area was 0.2 cmm2 (see Methods). Thus, on average, our experimental rates of snail removal of leaf material may be twice as great as would occur during snail activity in the marsh where the snails were collected. Note, however, that number of snails per individual cordgrass shoot was not uniform in the marsh; it ranged from 0 to 10 in our census plots, meaning that snails * cm-2 dead leaf ranged up to 0.7, a factor of 1.8 greater than our experimental value.

Our larger experimental snails removed organic mass from dead leaves at a rate of 42;b per 6 days (Fig. 1). This was close to the average organic-removal rate by L. i~roru~ff found in a similar, earlier experiment (August, 1992) in which snails were present per unit area of leaf at a 757; lower density (23% removed in 4 days; New- ell & Barlocher, unpubl.). If: (a) snails are active whenever leaves are wet (unpubl. obs.); (b) leaves in the marsh are wet SOS< of the time (Newell & Fallon, 1991); and (c) only half our present experimentaf rate is applicable to marshes containing 450 visible snails rnw2 (p revious paragraph, and Methods), then in 2 wk, the single dead leaf per shoot would lose 24% of its organic mass to snail grazing. Since snails aggregate (previous paragraph) and may move from shoot to shoot (they do not “home”: Vaughn & Fisher, 1992) seeking prime food sources, our experimental rates may be applicable to the field; in this case, 43’4 of organic mass would be removed from leaves over a 2-wk period. This may have been the principal reason that average number of standing, unshredded leaves per shoot was greater (3.8 i 0.6 versus 1 .O k 0.7) in our collecting marsh that did not contain visible (non-hidden) snails. Aggregation and consequent magnification of feeding effects is known for other littorinid snails (Norton et al., 1990).


Our larger experimental snails removed 69% of leaf ergosterol over a 6-day period.

Given the same assumptions as in the previous paragraph, snails in the marsh where

we collected our larger periwinkles would remove 55% of initial dead-leaf ergosterol

over a 2-wk period if grazing at our experimental rates. This may provide at least a

partial explanation for the large difference found between maximum ergosterol con-

centrations when snails were present (Newell et al., 1989) and when they were absent

(Newell & Fallon, 1991) (about 160 versus 525 pg.g-r organic mass for autumn co-

horts of leaves). This, along with production by a high-ergosterol species (B. spartinae:

Newell et al. [ 19871, and see Results), may explain why ergosterol content of standing-

dead leaves in our collecting marsh containing no visible snails was relatively high

(average = 934 pg. g-’ organic mass).

ACKNOWLEDGEMENTS

Financial support for this research was received from the National Science Foun-

dation (grants BSR-8604653, OCE-8600293, and OCE-9115642) and the Visiting-

Scientist Program of the Sapelo Island Research Foundation. UGMI Cont. No. 727.

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