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Aquatic macroinvertebrate communities of natural and ditched potholes in a San Francisco Bay salt marsh
Estuarine,
Coastal
and Shelf
(1985) 20,331-347
Science
Aquatic Macroinvertebrate Communities of Natural and Ditched Potholes in a San Francisco Bay Salt Marsh
Mark
A. Barnby,
Division of Entomology CA 94720, U.S.A. Received
17 December
Joshua
N. Collins
and Parasitology,
and Vincent
University
1983 and in revised
form
18 May
Keywords: salt marshes; salt pans; invertebrata; diversity; San Francisco Bay
of California,
H. Resh Berkeley,
1984
macrobenthos;
biomass;
Differences in macroinvertebrate community structure and composition were examined from April 1980 to March 1981 in three potholes that had been ditched for mosquito control and three natural (i.e. unditched) potholes, which are located in a San Francisco Bay, California, U.S.A. salt marsh. Measurements of incipient tidal flooding into potholes (i.e. pothole inundation threshold) indicated that these sites comprise a gradient of tidal influences. Exponential decreases in the frequency and duration of tidal inundation corresponded to linear increases in inundation threshold. Since ditched study sites had low thresholds they tended to be more uniformly and regularly influenced by tides, were less saline, had less variable temperature regimens, and supported less filamentous algae than natural potholes. Habitat conditions were generally more similar among ditched than unditched potholes, but environmental conditions were most severe at natural sites near the upper limit of the inundation threshold gradient, where some potholes desiccate during the dry season each year. Differences in macroinvertebrate communities corresponded to differences in habitat conditions. Species richness and diversity (Simpson’s Index) were generally highest near the middle of the inundation threshold gradient, which is a pattern predicted by the Intermediate Disturbance Hypothesis. Analysis of fauna1 composition using discriminant functions indicated more similarity among potholes located at the lowest positions of the inundation gradient than among potholes with intermediate thresholds. Since ditching lowers the inundation thresholds of potholes, it reduces species richness and diversity, while increasing fauna1 similarity. As a result, extensive ditching to control salt marsh mosquitoes can reduce the overall complexity of lentic macroinvertebrate communities.
Introduction salt marshes contain a variety of lentic environments, many of which are breeding sites for mosquitoes. In North American salt marshes, man-made mosquito control ditches have been used extensively to increase tidal flux in habitats where salt marsh mosquitoes oviposit, or to drain such habitats, and thereby create unfavorable conditions for the survival of mosquito eggsand larvae (Smith, 1904; Resh & Balling, 1983~). In
Tidal
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0 1985 Academic Press Inc. (London)
Limited
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M. A. Barnby,J.
N. Collins & V. H. Resh
some salt marshes, ditches might also allow predatory fish to gain accessto habitats containing mosquito larvae (Connell, 1940; Balling et al., 1980). Very little is known about the effects of ditches on non-target macroinvertebrate speciesthat coexist with salt marsh mosquitoes. Greenstone (1983) who studied predation of lentic invertebrates by the wolf spider Pardosa ramulosa (McCook) in a salt marsh near San Francisco Bay, California, stated that ditches result in a depauperate insect fauna, because ditches increase the flushing action of the tides. In contrast, Resh & Balling (1983b) indicated that ditches in San Francisco Bay Area salt marshesincrease habitat for at least one lentic insect species,the water boatman Trichocorixa reticuluta (Guerin-Meneville). Studies of the effects of mosquito control ditches on aquatic macroinvertebrate populations and communities may be essentialfor a general understanding of salt marsh ecology, since lentic habitats and mosquito control ditches are prominent hydrologic features of most North American salt marshes. Also, ditches are known to influence other biotic components of the salt marsh ecosystem. For example, in salt marshes around San Francisco Bay, ditching has been shown to affect the population density and community structure of terrestrial invertebrates (Barnby & Resh, 1980; Balling & Resh, 1982), the community structure of terrestrial plants (Balling & Resh, 1983), the abundance of a resident song sparrow (Collins & Resh, 1985), and both the population density and speciesrichness of estuarine fish (Balling et al., 1980). Therefore, in order to provide information about the response of lentic macroinvertebrates to ditching, we designed a study to compare macroinvertebrate community structure in ditched and natural (i.e. unditched) potholes.
Materials
and methods
Study area
Petaluma Marsh is a 1145ha salt marsh located along the Petaluma River, 10 km north of San Francisco Bay, California (Figure 1). Overall, the marsh surface is a flat landscape that approximately corresponds to the mean height of the higher high tides (MHHW). The marsh flora is dominated by pickleweed, Salicornia virginica L., which tends to monopolize salt marsh surfacesat elevations near the MHHW tidal datum (Hinde, 1954; Atwater et al., 1979). The elevational successionof plant zones typical of other, higher gradient salt marshesis not evident at Petaluma Marsh, except along its largest sloughs and immediate periphery. The marsh was extensively ditched by the Marin-Sonoma Mosquito Abatement District over a seven-year period, beginning in 1969. The water levels of lentic habitats in the marsh are affected by rainfall, a mixed tidal pattern (Marmer, 1951), and seasonalriver discharge. In northern California, the wet seasontypically lasts from November through April. However, during our sampling year, 92”, of the rainfall in the marsh occurred from January through June. Therefore, we have designatedthese six months asthe wet season. Since elevations of the marsh surface differ only slightly from MHHW, only the highest tides of the biweekly springtide seriescan inundate the marsh entirely. Although the highest annual tides generally occur in January and July, the marsh is frequently inundated during June, August, and December. Therefore, the lentic habitats are most likely to desiccate during October and early November, when both tidal inundation and rainfall are least likely to occur. During some winters, flood waters from the Petaluma
Aquatic
macroinvertebrate
communities
Figure 1. Location of study area, six main study sites (Dl-D3, Nl-N3), threshold sites (HS), and tide gauge. Examples of ponds, mosquito control natural tidal channels of different orders are also indicted.
333
five highest ditches, and
River cover the marsh for consecutive tidal cycles. However, no such flooding occurred during our sampling period, a year in which rainfall was well below average. The marsh surface is principally characterized by two types of lentic habitats, ponds and potholes. Ponds are relatively large basins surrounded by chronically saturated peat soil at the headwater areas of drainage systems. Ponds generally do not produce mosquitoes and seldom are ditched. Potholes (i.e. the channel pans of Yapp et al., 1917) are relatively small bodies of water and are remnants of first-order tidal channels. Under natural conditions, some potholes receive tidal water via subterranean ports, which represent the final stage of channel senility. Other, generally older potholes no longer contain ports and receive tidal water only during inundation of the surrounding marsh surface. These older potholes constitute most of the breeding habitat for salt marsh mosquitoes. Consequently, most of the older potholes in Petaluma Marsh are connected by mosquito control ditches to second- or higher-order natural tidal waterways (Figure 1). The following analysis of ditch effects involves only comparisons among older potholes. Study
sites
Our studies were concentrated among three ditched and three natural potholes, which are collectively referred to as the main study sites. In addition to these sites, we routinely examined five other natural potholes that are among the highest elevation lentic environments in the marsh. All eleven sites are close to one another and are similar in size, relative to the maximum size range for older potholes in the study area (Figure 1). However,
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&
V. H. Resh
-I -100
t50
-50
Elevation
relative
to MHHW
(cm)
Figure 2. Cumulative frequency distribution for the high tides at the center of Petaluma Marsh, relative to the inundation thresholds of the study sites, based upon continuous empirical tidal measurements for the duration of the sampling year (April 1980 to March 1981). For example, the figure shows that about 309b of all the high tides inundated all three of the ditched sites.
following an inundating tide, ditched sites were shallower than natural sites (2.5-7.5 cm compared with 20-30 cm). Empirical measurements of the times and heights of tides in a slough near the study sites (Figure l), when combined with records of exact moments of site inundation, indicated that each study site has a unique inundation threshold. Each threshold represents both the actual elevation of a site and the time necessary for tidal water to travel over the marsh surface or through a ditch. Therefore, two sites that are at the same elevation but at different distances from their common source of tidal water will have different inundation thresholds. In order of increasing threshold, the study sites were labelled D 1, D2, D3, Nl, N2, N3, and HS, with the letters D and N designating ditched and natural main sites, respectively, and HS designating the highest threshold sites (Figure 1). The lower three potholes (i.e. Dl-D3) were ditched in 1976. Tidal regimens vary predictably along the inundation threshold gradient. For example, thresholds for the ditched sites represent positions near mid-tidal range, where changes in tidal regimen per unit change in elevation are greatest (Figure 2). However, about 30% of all the high tides inundated all of the ditched sites. In contrast, most thresholds for the natural sites correspond to positions above the MHHW tidal plane, where tidal inundation is relatively infrequent and short in duration (Figure 2, Table 1).
Aquatic macroinvertebrate
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335
TABLE 1. Characteristics of the tidal regimens of the main ditched (Dl-D3), natural (Nl-N3), and highest threshold (HS) study sites, based upon continuous measurements for the duration of the sampling year (April 1980 to March 1981)
Site
Threshold to MHHW
Dl D2 D3 Nl N2 N3 HS
relative (cm)
-15 - 14 -5 0 f10 f15 f20
No. of inundations per year 328 318 261 210 98 56 41
main tidal
Total hours of inundation per year 1170 1090 780 605 245 110 70
All of our study sites supported floating, aquatic vegetation, at least during part of our sampling year. This cover was dominated by green algae, including Enteromorpha cZathrata (Roth) Grev., Ulothrix j&zcca (Dillw.) Thur., and Ulva sp. Some sites also supported small amounts of widgeon grass, Ruppia maritima L., which was the only macrophyte among our study sites. Environmental
data
Preliminary field work was begun in November 1979; quantitative data were collected from April 1980 to March 1981. Water salinity within each study site was measured weekly with a refractometer. Weekly values for the duration and frequency of tidal immdation were derived from the continuous record of the tide gauge. Visual estimatesof the percent aquatic plant cover at each main site were made weekly. In situ max/min thermometers were used to measure weekly temperature extremes at the main sites. In the summer of 1980, thermographs were installed at two adjacent potholes, one ditched and one natural, to determine the effects of tidal inundation on pothole temperature. The thermographs were used over a complete lunar cycle (10 August to 10 September 1980). Biological
data
During the year of data collection, three 180-cm2 sampleswere taken monthly at each main site. On two of the twelve sampling dates, sampleswere taken at high tide; at all other times samples were taken during slack low tide. All samples were taken at the centers of randomly selectedquadrats, and no quadrat was selectedmore than once. In sampling, a l-m long, 15.25-cm diameter PVC pipe was thrust 5 cm into the pothole substrate, then removed by covering the pipe bottom and lifting upward. Since we had established that the bottom 4 cm of a sample were composed of anoxic substrate that contained no living organisms, only the water and the uppermost 1 cm of substrate were retained for processing. Each sample was washed consecutively through sieveswith 2 mm (no. lo), 1 mm (no. 18), and 500 p (no. 35) pore sizes. The washed material was then floated on saturated salt solution to facilitate the sorting of specimens.The biomassof a samplewas determined by oven-drying to constant weight at 105 “C; prior to weighing, sampleswere cooled with dehydrated air. Analysis
Simple linear regression was used to measure how each environmental factor varied along the inundation threshold gradient. We used two-way analysis of variance to test
336
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30 . G < 0 h'
A. Barnby,J.
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& V. H. Resh
.
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(bi
2
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1’ DI D2 -15 -14
1 D3 -5
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1 N3 t15
lnundatlon
I HS t20 threshold
I II DI D2 -15 -14 relative
I 02 -5
I NI 0
to MHHW
(cm)
I N2 HO
I N3 fl5
I HS t20
Figure 3. Relationships between inundation threshold and weekly temperature range for (a) wet and (b) dry seasons. For the wet season, dashed line represents weeks with at least 1.25 cm rainfall; solid line represents weeks with less rainfall.
the hypotheses that neither seasonal biomass nor species diversity (Simpson’s Index, sensu Routledge, 1979) differed between the ditched and the natural potholes. Linear discriminant analysis (Klecka, 1975) was used to measure the similarity of physical conditions and fauna1 composition among the main sites, and to determine if any species assemblages were indicative of particular inundation thresholds or pothole conditions. Discriminant analysis reduced each data case (i.e. a set of date- and sitespecific measurements of physical parameters or population densities) to a single summary index (i.e. the discriminant score). Each case was then reassigned, according to its score, to one of the six main sites, with the discriminant functions minimizing the probability of incorrectly reassigning data. The absolute magnitudes of the discriminant function coefficients, which weight each variable in a case, were used to identify the species or physical parameters that were most important for correctly classifying cases. The mean discriminant score (i.e. the centroid) for each site was plotted, using the discriminant functions to calculate Cartesian coordinates. Physical and fauna1 similarities among the sites were then inferred from the relative positions of the centroids. Results The
and discussion
environment
of a pothole
The physical data indicate that the environment of a pothole varies according to its inundation threshold. For example, weekly pothole temperature range descreased with increasing threshold for the wet and dry seasons [Figure 3(a), (b), respectively]. This is because temperatures in ditched potholes are regularly influenced by the tides, which both import and export heat. Night-time flood tides, which in general are warm relative to the soil and air, and the relatively cool daytime flood tides exchange less heat with the air and soil while traveling through a full ditch than when traveling as a thin sheet of water over the marsh surface (Felton, 1978). As a result, temperature differences between water already in a pothole and the incoming tidal water are greater for the
Aquatic
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337
communities
(b)
I
Site
lnundotlon
threshold
II DI D2 -15 -14
relatwe
I D2 -5 to MHHW
1 NI 0
I N2 +I0
I N3 t15
I HS +20
(cm)
Figure 4. Relationships between inundation threshold and variability of temperature range for (a) wet and (b) dry seasons. Variability is reported as the monthly coefficient of variation calculated from weekly temperature ranges.
ditched than the natural study sites. Also, when tides recede from the marsh surface, ditched potholes are nearly drained, and the remaining shallow water rapidly exchanges heat with the atmosphere. Thus, both frequent inundation and changes in water level can cause ditched potholes to have broad temperature ranges during short (i.e. 1 week) time periods. When longer periods of time (i.e. 1 month) were considered, the variability of weekly temperature range was positively correlated with inundation threshold for both the wet and dry seasons [Figure 4(a), (b), respectively]. This is because regular inundation reduces the influence of atmospheric temperatures, which vary more than the temperatures of the tides. Among all the study sites, salinity was lower and more uniform in the wet season than in the dry season [Figure 5(a), (b)], b ecause wintertime increases in rainfall and river discharge reduced salinities throughout the marsh. During the dry season, the more frequent tidal flushing in ditched potholes generally prevented salt accumulation, whereas in natural potholes low rates of flushing allowed salts to concentrate. Among potholes with similar tidal regimens, those covered with thick algal mats had higher salinities than those lacking such cover. For example, the scant algal cover in pothole Nl [Figure 6(a)] was probably responsible for its low salinities relative to D3, a site which had a slightly lower inundation threshold but much greater algal cover [Figure 6(b)]. Since a filamentous algal mat increases pothole surface area, the mat can also increase evaporative water loss, and thus increase pothole salinity. At Petaluma Marsh, evaporative losses due to algal mats might be accelerated by afternoon winds that reduce the water vapor pressure at the marsh surface. This influence of algae on salinity may be responsible for the low, but significant positive correlation between inundation threshold and weekly maximum salinity for the dry season (r=0.25; P
338
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Q
V. H. Resh
(a) 140
Figure highest
1
I I I I I I I I Nov JUI Sep May 5. Seasonal patterns of change in salinity threshold sites (HS), and (b) ditched study
II Jar
11 I
Mar
for (a) natural sites.
sites including
the
tidal regimen, algal cover, evaporation, and precipitation caused fluctuations in pool salinities in a salt marsh located near the Bay of Fundy, Nova Scotia. In contrast, Ward & FitzGerald (1983~) found that temperature in a Quebec salt marsh was the major factor controlling pool salinities, although algal cover did not differ among the pools they studied. Percent algal cover was positively correlated with inundation threshold, especially in the dry season (r = 0.60; P < 0.0 1). However, algal cover was highly variable, even among study sites with similar thresholds. Although our data do not indicate reasons for the variable distribution of algae among the natural sites, some mechanisms for cover reduction at potholes with low thresholds can be inferred. For example, relatively high frequencies of tidal flushing may have disrupted the algal mats and caused their export. A similar mechanism was suggested for the lack of an established algal cover in a low elevation pool in a Quebec salt marsh (Ward & FitzGerald, 1983~). Our analysis of abiotic parameters suggests that high threshold potholes are environmentally severe habitats for macroinvertebrates. In potholes with high
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100 75
macroinvertebrate
339
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Figure sites.
6. Percent
algal cover
Sep of water
Nov
surface
Jan
for (a) natural
Mar
and (b) ditched
TABLE 2. Mean values* S.D. of total macroinvertebrate community for natural and ditched potholes in the wet and dry seasons
Natural Wet season Dry season
0.061+ 0.045
main study
biomass
(gm-‘)
Ditched 0.041
& 0.045
0,056 0.043
k 0.043 k 0,032
thresholds, infrequent tidal inundation can result in very high salinities and habitat desiccation. Although temperatures can be extreme for low threshold potholes, thermal regimens are more variable for potholes with high thresholds. Therefore, any aquatic macroinvertebrate populations living in high threshold potholes will be subject to environmental conditions that involve very high salinities, insufficient moisture, and irregular and unpredictable changes. Community
parameters
Biomass
Wet season community biomass was significantly higher than dry season biomass (P = 0.05) in both the natural and ditched sites, whereas differences in biomassbetween ditched and natural sites were not significant for either season(P=O.71; Table 2). The higher invertebrate biomass during the wet seasonmay have resulted from increased food resources. For example, we observed that most algal mats began decomposing in early winter, when detritivores dominated the pothole fauna. Similarly, Cameron (1972) reported that organic debris increased during wintertime in a nearby salt marsh, and this
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material provided a large food source for invertebrate detritivores. We alsoobserved that macroinvertebrates did not feed on viable algal mats, and infer that the healthy algal mats that occurred during summer were more important asmicrohabitat than as food. Species richness
The species richness of the aquatic macroinvertebrate fauna of Petaluma Marsh is apparently higher than that reported for other salt marshes. Nicol (1935) collected 13 species of insects in an English salt marsh; Campbell & Denno (1978) collected 20 speciesof insects in a New Jersey salt marsh; Kelts (1979) collected 19 speciesof insects in a New Hampshire salt marsh; and Ward & FitzGerald (1983~) collected 12 speciesof insects in a Quebec salt marsh. At Petaluma Marsh we collected 60 166 specimens representing 32 taxa of macroinvertebrates, of which 24 taxa were insects (Table 3). However, results from these studies are not strictly comparable, since different sampling methods were used. Our study also revealed a much richer insect fauna for Petaluma Marsh than previously described by Greenstone (1978), but he did not actually sample the pothole invertebrates. In addition, the collection of 8322 insect specimens that comprised 18 taxa from our three ditched study sites disagrees with the assertion by Greenstone (1983) that ditched potholes in Petaluma Marsh are devoid of aquatic insects. Speciesrichness was always higher for sitesNl through N3 than for either the ditched or the highest elevation sites (Figure 7). This pattern may be a function of changes in either the disturbance rate or habitat severity along the inundation threshold gradient. Among low threshold potholes, tidal disturbances (i.e. sediment transport, algal export, and changesin water level, salinity, and temperature) are frequent, whereas severe conditions (i.e. very high salinities and desiccation) are most probable among potholes with the highest thresholds. According to the ‘ Intermediate Disturbance Hypothesis ’ (Connell, 1978), speciesrichness is greatest where rates of habitat disturbance or habitat severity are intermediate. In our study, plots of richness versus inundation threshold for both the wet and dry seasons[Figure 8(a), (b)] resemble the relationship predicted by Connell (1978). Other studies have shown that marine invertebrate speciesdiversity is greatest where disturbance rates are not extreme (e.g. Levin & Paine, 1974; Sousa, 1979). Species diversity
During both the wet and dry seasons,speciesdiversity was significantly higher for the natural than the ditched potholes (P < 0.01); however, no significant seasonaldifferences were found (P=O.81; Table 4). The patterns of speciesdiversity among our study sites reflected differences in abundances of the most common taxa, which corresponded to environmental differences along the threshold gradient. For example, the density of the most common invertebrate, the oligochaete Paranais litoralis (Miiller) (Figure 9), was both directly and indirectly influenced by environmental factors. In potholes Dl and D2, the amount of filamentous algaewas insufficient to serve asrefuge for P. litoralis. As a result, P. 1itoraZis was probably consumed in large numbers by the secondmost common macroinvertebrate, the water boatman T. reticulata, which is at least a facultative consumer of small animals (Carpelan, 1957; Davis, 1966; Cox, 1969). In potholes D3 and Nl, however, large numbers of P. litoralis were probably able to avoid predation by inhabiting filamentous algae. This conclusion is based on repeated observations that algal mats typically contained large numbers of P. litoralis, whereas nymphs and adults
Aquatic
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communities
3. Fauna collected at all study sites during wet and dry seasons in Petaluma Salt Marsh. For the natural and ditched main sites, counts are totals per season. Only presence (+) or absence of species is indicated for the highest threshold sites
TABLE
Natural wet Polychaeta
sp.
Oligocheata Lumbriculus lineatus Miiller Paranais litoralis (Miiller) (these counts include Tubijicoides nethoides (Brinkhurst) and two undescribed species of Rhyacodrilinae, all of which are rare taxa in samples)
Ditched wet
dry
8 55 11192
Highest dry
wet
13
6
113 12 7287 20716
58 5982
23
Crustacea Tanais vanis Miller Anisogammarus confer&ohs (Stimpson)
12
5
23
5
1552
196
198
35
Insecta Hemiptera Trichocorixa reticulara (Guerin-Meneville)
867
1957
1201
5859
Diptera Chironomus sp. Cricotopus sp. Hydrobaenus sp. Dasyhela sp. Psychoda salicornia Quate Aedes dorsalis (Meigen) Aedes squamiger (Coquillett) Dolichopus sp. Eristalis tenax Linnaeus Tabanus laticeps Hine Odontomyia sp. Chiromyzinae sp. Ephydra millbrae Jones Lamproscatella muria Matis Scatella stagnalis Fallen Paracoenia bisetosa (Coquillett) Hydrellia griseola (Fallen) Canace sp. Cyclorrhapha sp.
83 101 3 43 3 4 2 35 9 0 41 1 242 32 0 0 1 0 5
0 0 0 21 2 0 0 95 6 0 16 1 344 16 1 0 1 1 3
0 8 1 73 252 0 0 45 1 0 4 2 253 5 1 3 0 40 1
0 0 3 21 138 0 0 34 1 1 1 0 223 19 0 0 0 3 0
Coleoptera Enochrus diffusus (Le Conte) Berosuspunctatissimus Le Conte Tropisternus salsamentus Fall Ochthebius rectus Le Conte
236 16 0 13
147 0 3 2
87 0 0 3
39 0 0 0
dry
+
+ +
+
of T. reticulata were never observed within these mats. Among potholes with higher thresholds, harsh conditions (i.e. high salinity and frequent desiccation) may have directly limited the density of P. litoralis. For example, low numbers of P. litoralis were sampled in pothole N3, although filamentous algae were abundant and T. reticulata was scarce.
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HS ---->
2-
1
0-N I
w
I
&
V. H. Resh
,-
b----c----
I JUl
I
I Sep
I
I Nov
I
‘\-’ I JCUl
Figure 7. Temporal patterns of species richness study sites and highest threshold sites (HS).
fj-
I
I Mar
for ditched
(D) and natural
(N)
main
(0) -
6-
I
4-
2-
I
I I DI 02
I D3
I NI
I N2
I N3
I HS
Figure 8. Relationship between species richness and environmental severity or rate of habitat disturbance as represented by inundation threshold (i.e. relative positions along the abscissa reflect height above MHHW) for (a) wet and (b) dry seasons. Means and error bars for the highest threshold sites are based upon weekly collections. TABLE 4. Mean values& 1 S.D. of total macroinvertebrate community diversity (Simpson’s index) for natural and ditched potholes in the wet and dry seasons Natural Wet season Dry season
1.04+051 1.12kO.59
Ditched 0,70+0.32 0,66*0.37
Aquatic macroinvertebrate
$ I :::;I May Jul
Figure
Sep
Nov
communities
Jon
Mar
343
May JUI
Se0
Nov
9. Temporal patterns of the abundance (log,,) of P. litoralis reticulata( W -- n ), and A. confervicolus (A A), at the main study sites are represented by graphs (a)-(c); ditched sites by graphs (d)-(0.
Jan
Mar
(O-a), T. sites. Natural
Two environmental factors probably allowed populations of T. reticulata to attain very high densities, such as those which occurred in the two lowest threshold ditched sites and in the lowest threshold natural site (i.e. Dl, D2, Nl; Figure 9). First, frequent inundation reduced the risk of habitat desiccation and the consequential stranding of immature, wingless water boatmen (Balling & Resh, 1984). Second, since these three potholes contained relatively small amounts of floating algal cover [Figure 6(a), (b)], they were probably more intensively colonized by aerial adult water boatmen. This is because adults that alight on algae tend to explore it briefly, then take flight, whereas those that land in open water tend to remain. Increased water salinities were apparenty not a factor in reducing the numbers of T. reticulata in potholes with high inundation thresholds, since dense populations have been observed in high threshold potholes that were devoid of algal cover and where water salinities were two to four times asconcentrated as seawater. Also, Carpelan (1957) found the highest population densities of this species in very saline (i.e. 63%0) salt evaporation ponds located adjacent to southern San Francisco Bay. The spatial and temporal occurrence of the third most common invertebrate, the amphipod Anisogammarus confervicolus (Stimpson) (Figure 9), might also have been directly affected by conditions of algal cover. That is, populations of A. confervicolus were most abundant during the wet season, and were essentially restricted to high threshold potholes containing large amounts of deteriorating filamentous algae. Since A. confervicolus is a detritivore, the decomposing algal mats probably served as a food resource. A similar relationship between occurrence of A. confervicolus and filamentous algae was observed by Carpelan (1957) in salt evaporation ponds near southern San Francisco Bay. In the above discussion, we suggestthat many of the differences in macroinvertebrate community structure that we observed among potholes in Petaluma Marsh were due to differences in abiotic factors and algal cover. This is in contrast to Campbell & Denno (1978), who ascribed spatial differences in invertebrate community structure among unditched potholes in a New Jersey salt marsh to predation by birds and fish. However,
M. A. Barnby,J.
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(a) NI .
NI .
DI . .
D2
l
N3 .
.
N2
D3
.
D3 .
Monthly
lnundatlon
frequency
Figure 10. Plots of (a) wet and (b) dry season main site discriminations based upon environmental parameters. Each site is represented by its centroid (see methods). The most discriminating factors of the first and the second functions are given as labels for the abscissa and ordinate, respectively. Distances among centroids parallel to either axis indicate absolute differences; the axes do not indicate direction of increase or decrease in paremeter value.
these salt marsh pools may be less variable as habitats, and therefore might support invertebrate communities that are lessregulated by physical factors than the communities in Petaluma Marsh. Signs of bird visitation were rare among our study sites, and we infer that predation by birds generally did not influence the structure of the macroinvertebrate communities. Furthermore, at Petaluma Marsh the invasion of potholes by large numbers of fish was apparenty both spatially and temporally uncommon, and probably did not affect macroinvertebrate community structure. In fact, we observed fewer than 50 fish among our study sites during more than 150h of reconnaissancespanning 12 consecutive months. Almost all of these fish were threespine stickleback, Gasterosteus aculeatus L., which apparently only invade potholes during tidal inundation and feed almost exclusively on microcrustacea (Balling, unpublished data). In addition, caged experiments in a salt marsh pool in Quebec indicated that G. aculeatus had no measurable impact on the macroinvertebrate community (Ward & FitzGerald, 1983b). Environmental
and fauna1 similarity
The environment
Based upon environmental factors, the discriminant functions correctly classified 89U,, and 86% of the data casesfor the wet and the dry seasons,respectively. This indicates successful classification relative to the 16y; chance (1 in 6) of randomly assigning the data casesto the correct study sites. Incorrect classification of casesoccurred mainly among potholes with similar inundation thresholds. The discriminant analysis basedupon environmental factors indicated that each main site was environmentally unique, but that those sites that have the most similar inundation thresholds were also most similar with regard to temperature, tidal regimen, salinity, and percent plant cover. For example, although the percent correct classification was always high, the centroids for potholes Dl and D2 were consistently plotted together, as were centroids for potholes N2 and N3 [Figures 10(a), (b)]. Although the centroids for the two sites with intermediate thresholds (i.e. D3, Nl) were plotted apart from one another, they were consistently plotted between the centroids for the higher and lower threshold sites. These four sites (i.e. Dl, D2, N2, N3) were primarily distinguished by differences in inundation threshold, whereas the sites with intermediate
Aquatic
communities
macroinvertebrate
(0)
345
(b)
N3
Nl . . D2 l
N3 .
03
l
.D3 N2 .
61
DI ’
b2
r;l r;2 Monthly
density E. DlffUWS
of
Monthly Doltchopus
density of and E. teenox
Figure 11. Plots of (a) wet and (b) dry season main site discriminations based upon fauna1 composition and species density. Each site is represented by its centroid (see methods). The more important taxa of the first and second discriminating functions are given as labels for the abscissa and ordinate, respectively. Note that the axes only show absolute differences; the direction of increase or decrease in species density is not indicated.
thresholds (i.e. D3, Nl) were distinguished mainly by differences in salinity [Figures 10(a), (b)]. The pattern of classification for sitesD3 and Nl probably reflects the higher salinities causedby the greater algal cover in site D3 relative to site Nl. The fauna
If the macroinvertebrate species assemblagesof potholes are indicative of discrete positions along the inundation threshold gradient, then the study sites can be classified according to their fauna1characteristics, and the pattern of classification (i.e. the relative positions of the centroids in the discriminant function plots) should resemble that based upon the environmental features. Using population densities of all speciesas variables, 72:/b and 67% of the caseswere classified correctly for the wet and dry seasons,respectively. Again, this indicates successful classification relative to the 16:& chance (1 in 6) of randomly assigning data cases to the correct study sites. Also, the centroids for the sites generally were plotted according to their position along the threshold gradient [Figure 1l(a), (b)]. For both seasons, the centroids for the ditched potholes were grouped together and the centroid for the next higher pothole (i.e. Nl) was plotted nearby. The centroids for the two siteswith the highest thresholds (i.e. N2, N3) were plotted apart from each other and the rest. These results indicate that ditched and natural potholes with different inundation thresholds below MHHW (e.g. Dl-Nl) support similar macroinvertebrate faunas, whereas potholes with different thresholds above MHHW (e.g. N2, N3) support faunas that are more distinct. Furthermore, since physical conditions were similar for potholes N2 and N3 [i.e. basedupon physical factor centroids; Figure 10(a), (b)], the distinctiveness of their faunas suggests that slight differences in threshold (e.g. 5 cm) above MHHW can result in relatively large differences in speciescomposition and population density. Rare taxa, found primarily at sites Nl-N3, were important in distinguishing these sites from the ditched sites. For the wet season[Figure 1l(a)], the most important discriminators were Enochrus difluusus(Le Conte) larvae and adults, and larvae of the chironomid genera Cricotopus and Chironomus. For the dry season[Figure II(b)], the most important taxa were Dolichopus larvae, larvae of the rat-tailed maggot Eristalis tenax L., and larvae of E. diffusus.
346
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Conclusions Although the surface of Petaluma Marsh approximately corresponds to the mean height of the higher high tides (MHHW), an elevational gradient from at least 15 cm below MHHW to 20 cm above the tidal datum is represented by the inundation thresholds of potholes. Both the frequency and duration of tidal inundation among salt marsh lentic environments decrease exponentially with linear increases in inundation threshold. However, habitat conditions are most variable among potholes with intermediate thresholds that approximately correspond to MHHW, where slight differences in threshold can result in ecologically significant differences in salinity and moisture. In Petaluma Marsh, macroinvertebrate community structure and fauna1 composition vary among potholes according to differences in habitat conditions, which are regulated by the tides. For a given season, species richness is lowest and fauna1 composition is most similar among potholes that have very high (i.e. > 15 cm above MHHW) inundation thresholds, and therefore have environmental conditions that tend to be extreme. Among potholes with very low thresholds (i.e. < 10 cm below MHHW), habitat conditions are relatively simple, invariant, and not severe; consequently, species richness and diversity are relatively low, and fauna1 composition is similar throughout the year. Among potholes with intermediate thresholds (i.e. near MHHW), significant differences in habitat conditions correspond to slight differences in threshold. Fauna1 composition is most variable among these potholes, and species richness and diversity are relatively high. When a pothole is ditched, its inundation threshold is lowered, usually from an intermediate position near MHHW, to a new position much below that tidal datum. Consequently, its environmental characteristics and the macroinvertebrate community that it supports becomes less complex and more indicative of a broad range of lower elevation tidal regimens. Since ditched potholes are more numerous than ponds and natural potholes combined, a large proportion of the lentic habitats in Petaluma Marsh probably support macroinvertebrate communities that are now simpler and more alike one another than they were prior to ditching. Acknowledgements We thank S. S. Balling for project assistance and R. 0. Brinkhurst for oligocheate identifications. Support for this project was provided by University of California Mosquito Research Funds. References Atwater, B. F., Conrad, S. G., Dowden, J. N., Hedel, C. W., MacDonald, R. L. & Savage, W. 1979 History, landforms and vegetation of the estuary’s tidal marshes, pp. 347-385. In San Francisco Bay: The Urbanized Esruarv (Conomos, T. T., ed). Pacific Division, American Association for the Advancement of Science, San Francisco, 493 pp.Balling, S. S. & Resh, V. H. 1982 Arthropod community responses to mosquito control recirculation ditches in San Francisco Bay salt marshes. Environmental Entomology 11,801-808. Balling, S. S. & Resh, V. H. 1983 The influence of mosquito control recirculation ditches on plant biomass, production, and composition in two San Francisco Bay salt marshes. Estuarine Coastal and Shelf Science 16, 151-161. Balling, S. S. & Resh, V. H. 1984 Life history variability in the water boatman Trichocorixa reticulara (Hemiptera: Corixidae) in San Francisco Bay salt marsh ponds. Annals of the Entomological Society of America 17,14-19.
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Balling, S. S., Sroehr, T. & Resh, V. H. 1980 The effects of mosquito control recirculation ditches on the fish community of a San Francisco salt marsh. California Fish and Game 66,25-34. Bamby, M. A. & Resh, V. H. 1980 Distribution of arthropod populations in relation to mosquito control recirculation ditches and natural channels in the Petaluma Salt Marsh of San Francisco Bay. Proceedings of the California Mosquito and Vector Control Association 48,100-102. Bleakney, J. S. & Meyer, K. B. 1979 Observations on saltmarsh pools, Minas Basin, Nova Scotia, 1965-1977. Proceedings of the Nova Scotia Institute of Science 29,353-371. Cameron, G. N. 1972 Analysis of insect trophic diversity in two salt marsh communities. Ecology 53,58-73. Campbell, B. C. & Denno, R. F. 1978 The structure of the aquatic insect community associated with intertidal pools on a New Jersey salt marsh. Ecological Entomology 3,181-187. Carpelan, L. H. 1957 Hydrobiology of the Alviso salt ponds. Ecology 38,375-390. Collins, J. N. & Resh, V. H. 1985 Utilization of natural and man-made habitats by the salt marsh song sparrow, Melospiza melodiu samuelis Baird. California Fish and Game (in press). Connell, J. H. 1978 Diversity in tropical ram forests and coral reefs. Science 199,1302-1310. Connell, W. D. 1940 Tidal inundation as a factor limiting the distribution of Aedes spp. in a Delaware salt marsh. Proceedings of the New Jersey Mosquito Extermination Association 27, 166-177. Cox, M. C. 1969 The biology of the euryhaline water boatman Trichocorixa reticulata (Guerin-Meneville) (Hemiptera-Corixidae). M.S. Thesis, California State University, San Diego. 84 pp. Davis, C. C. 1966 Notes on the ecology and reproduction of Trichocorixa reticulum in a Jamaican salt-water pool. Ecology 47,850-852. Felton, C. R. M. 1978 The energy budget of a south San Francisco tidal salt marsh. Ph.D. thesis, University of California, Berkeley, California. 322 pp. Greenstone, M. H. 1978 The numerical response to prey availability of Purdosa ramulosa (McCook) (Araneae: Lycosidae) and its relationship to the role of spiders in the balance of nature. Symposia of the Zoological Society of London 42, 183-193. Greenstone, M. H. 1983 Site-specificity and site tenacity in a wolf spider: A serological dietary analysis. Oecologia S&79-83. Hinde, H. P. 1954 Vertical distribution of salt marsh phanerograms in relation to tide levels. Ecological Monographs 24,209-225. Kelts, L. J. 1979 Ecology of a tidal marsh corixid, Trichocorixa verticalis (Insecta, Hemiptera). Hydrobiologia 64,37-57. Klecka, W. R. 1975 Discriminant analysis. pp. 434-467. In SASS, Statistica Package for the Social Sciences. Nie, N. H., Hull, C. H., Jenkins, J. G., Steinbrenner, J. and Bent, D. H. (eds). 2nd ed., McGraw-Hill Book Co., New York, 675 pp. Levin, S. A. & Paine, R. T. 1974 Disturbance, patch formation and community structure. Proceedings of the National Academy of Science (U.S.A.) II, 2744-7. Marmer, H. A. 1951 Tidal Datum Planes. Special publication no. 135, U.S. Dept. Commerce, U.S. Government Printing Office, Washington, D.C. 142 pp. Nicol, E. A. T. 1935 The ecology of a salt-marsh. Journal oj the Marine Biological Association of the United Kingdom 20,203-26 1. Resh, V. H. & Balling, S. S. 1983~ Ecological impact of mosquito control recirculation ditches on San Francisco Bay marshlands: Study conclusions and recommendations. Proceedings of the Cultfornia Mosquito and Vector Control Association 51,49-53. Resh, V. H. & Balling, S. S. 19836 Tidal circulation alteration for salt marsh mosquito control. EnvironmentaZ Management 7,79-84. Routledge, R. D. 1979 Diversity indices: Which ones are admissible? Journal of Theoretical Biology 76, 503-515. Smith, J. B. 1904 The common mosquitoes of New Jersey. Bulletin of the New York AgricuZturaZ Experiment Station 171, l-40. Sousa, W. P. 1979 Disturbance in marine intertidal boulder fields: the nonequilibrium maintenance of species diversity. Ecology 60, 1225-1239. Ward. G. & FitzGerald. G. 1. 1983a Macrobenthic abundance and distribution in tidal ~001s of a Quebec salt marsh. Canadi&3ournaZof Zoology 61, 1071-1085. Ward, G. & FitzGerald, G. J. 19836 Fish predation on the macrobenthos of tidal salt marsh pools. Canadian 3ournaZof Zoology 61, 1358-1361. Yapp, R. H., Johns, D. & Jones, 0. T. 1917 The salt marshes of the Dovey Estuary. Part II. The salt marshes.Journal of Ecology $65-103.
Coastal
and Shelf
(1985) 20,331-347
Science
Aquatic Macroinvertebrate Communities of Natural and Ditched Potholes in a San Francisco Bay Salt Marsh
Mark
A. Barnby,
Division of Entomology CA 94720, U.S.A. Received
17 December
Joshua
N. Collins
and Parasitology,
and Vincent
University
1983 and in revised
form
18 May
Keywords: salt marshes; salt pans; invertebrata; diversity; San Francisco Bay
of California,
H. Resh Berkeley,
1984
macrobenthos;
biomass;
Differences in macroinvertebrate community structure and composition were examined from April 1980 to March 1981 in three potholes that had been ditched for mosquito control and three natural (i.e. unditched) potholes, which are located in a San Francisco Bay, California, U.S.A. salt marsh. Measurements of incipient tidal flooding into potholes (i.e. pothole inundation threshold) indicated that these sites comprise a gradient of tidal influences. Exponential decreases in the frequency and duration of tidal inundation corresponded to linear increases in inundation threshold. Since ditched study sites had low thresholds they tended to be more uniformly and regularly influenced by tides, were less saline, had less variable temperature regimens, and supported less filamentous algae than natural potholes. Habitat conditions were generally more similar among ditched than unditched potholes, but environmental conditions were most severe at natural sites near the upper limit of the inundation threshold gradient, where some potholes desiccate during the dry season each year. Differences in macroinvertebrate communities corresponded to differences in habitat conditions. Species richness and diversity (Simpson’s Index) were generally highest near the middle of the inundation threshold gradient, which is a pattern predicted by the Intermediate Disturbance Hypothesis. Analysis of fauna1 composition using discriminant functions indicated more similarity among potholes located at the lowest positions of the inundation gradient than among potholes with intermediate thresholds. Since ditching lowers the inundation thresholds of potholes, it reduces species richness and diversity, while increasing fauna1 similarity. As a result, extensive ditching to control salt marsh mosquitoes can reduce the overall complexity of lentic macroinvertebrate communities.
Introduction salt marshes contain a variety of lentic environments, many of which are breeding sites for mosquitoes. In North American salt marshes, man-made mosquito control ditches have been used extensively to increase tidal flux in habitats where salt marsh mosquitoes oviposit, or to drain such habitats, and thereby create unfavorable conditions for the survival of mosquito eggsand larvae (Smith, 1904; Resh & Balling, 1983~). In
Tidal
331 0272-7714/85/030331+
17 $03.00/O
0 1985 Academic Press Inc. (London)
Limited
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N. Collins & V. H. Resh
some salt marshes, ditches might also allow predatory fish to gain accessto habitats containing mosquito larvae (Connell, 1940; Balling et al., 1980). Very little is known about the effects of ditches on non-target macroinvertebrate speciesthat coexist with salt marsh mosquitoes. Greenstone (1983) who studied predation of lentic invertebrates by the wolf spider Pardosa ramulosa (McCook) in a salt marsh near San Francisco Bay, California, stated that ditches result in a depauperate insect fauna, because ditches increase the flushing action of the tides. In contrast, Resh & Balling (1983b) indicated that ditches in San Francisco Bay Area salt marshesincrease habitat for at least one lentic insect species,the water boatman Trichocorixa reticuluta (Guerin-Meneville). Studies of the effects of mosquito control ditches on aquatic macroinvertebrate populations and communities may be essentialfor a general understanding of salt marsh ecology, since lentic habitats and mosquito control ditches are prominent hydrologic features of most North American salt marshes. Also, ditches are known to influence other biotic components of the salt marsh ecosystem. For example, in salt marshes around San Francisco Bay, ditching has been shown to affect the population density and community structure of terrestrial invertebrates (Barnby & Resh, 1980; Balling & Resh, 1982), the community structure of terrestrial plants (Balling & Resh, 1983), the abundance of a resident song sparrow (Collins & Resh, 1985), and both the population density and speciesrichness of estuarine fish (Balling et al., 1980). Therefore, in order to provide information about the response of lentic macroinvertebrates to ditching, we designed a study to compare macroinvertebrate community structure in ditched and natural (i.e. unditched) potholes.
Materials
and methods
Study area
Petaluma Marsh is a 1145ha salt marsh located along the Petaluma River, 10 km north of San Francisco Bay, California (Figure 1). Overall, the marsh surface is a flat landscape that approximately corresponds to the mean height of the higher high tides (MHHW). The marsh flora is dominated by pickleweed, Salicornia virginica L., which tends to monopolize salt marsh surfacesat elevations near the MHHW tidal datum (Hinde, 1954; Atwater et al., 1979). The elevational successionof plant zones typical of other, higher gradient salt marshesis not evident at Petaluma Marsh, except along its largest sloughs and immediate periphery. The marsh was extensively ditched by the Marin-Sonoma Mosquito Abatement District over a seven-year period, beginning in 1969. The water levels of lentic habitats in the marsh are affected by rainfall, a mixed tidal pattern (Marmer, 1951), and seasonalriver discharge. In northern California, the wet seasontypically lasts from November through April. However, during our sampling year, 92”, of the rainfall in the marsh occurred from January through June. Therefore, we have designatedthese six months asthe wet season. Since elevations of the marsh surface differ only slightly from MHHW, only the highest tides of the biweekly springtide seriescan inundate the marsh entirely. Although the highest annual tides generally occur in January and July, the marsh is frequently inundated during June, August, and December. Therefore, the lentic habitats are most likely to desiccate during October and early November, when both tidal inundation and rainfall are least likely to occur. During some winters, flood waters from the Petaluma
Aquatic
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communities
Figure 1. Location of study area, six main study sites (Dl-D3, Nl-N3), threshold sites (HS), and tide gauge. Examples of ponds, mosquito control natural tidal channels of different orders are also indicted.
333
five highest ditches, and
River cover the marsh for consecutive tidal cycles. However, no such flooding occurred during our sampling period, a year in which rainfall was well below average. The marsh surface is principally characterized by two types of lentic habitats, ponds and potholes. Ponds are relatively large basins surrounded by chronically saturated peat soil at the headwater areas of drainage systems. Ponds generally do not produce mosquitoes and seldom are ditched. Potholes (i.e. the channel pans of Yapp et al., 1917) are relatively small bodies of water and are remnants of first-order tidal channels. Under natural conditions, some potholes receive tidal water via subterranean ports, which represent the final stage of channel senility. Other, generally older potholes no longer contain ports and receive tidal water only during inundation of the surrounding marsh surface. These older potholes constitute most of the breeding habitat for salt marsh mosquitoes. Consequently, most of the older potholes in Petaluma Marsh are connected by mosquito control ditches to second- or higher-order natural tidal waterways (Figure 1). The following analysis of ditch effects involves only comparisons among older potholes. Study
sites
Our studies were concentrated among three ditched and three natural potholes, which are collectively referred to as the main study sites. In addition to these sites, we routinely examined five other natural potholes that are among the highest elevation lentic environments in the marsh. All eleven sites are close to one another and are similar in size, relative to the maximum size range for older potholes in the study area (Figure 1). However,
334
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N. Collins
&
V. H. Resh
-I -100
t50
-50
Elevation
relative
to MHHW
(cm)
Figure 2. Cumulative frequency distribution for the high tides at the center of Petaluma Marsh, relative to the inundation thresholds of the study sites, based upon continuous empirical tidal measurements for the duration of the sampling year (April 1980 to March 1981). For example, the figure shows that about 309b of all the high tides inundated all three of the ditched sites.
following an inundating tide, ditched sites were shallower than natural sites (2.5-7.5 cm compared with 20-30 cm). Empirical measurements of the times and heights of tides in a slough near the study sites (Figure l), when combined with records of exact moments of site inundation, indicated that each study site has a unique inundation threshold. Each threshold represents both the actual elevation of a site and the time necessary for tidal water to travel over the marsh surface or through a ditch. Therefore, two sites that are at the same elevation but at different distances from their common source of tidal water will have different inundation thresholds. In order of increasing threshold, the study sites were labelled D 1, D2, D3, Nl, N2, N3, and HS, with the letters D and N designating ditched and natural main sites, respectively, and HS designating the highest threshold sites (Figure 1). The lower three potholes (i.e. Dl-D3) were ditched in 1976. Tidal regimens vary predictably along the inundation threshold gradient. For example, thresholds for the ditched sites represent positions near mid-tidal range, where changes in tidal regimen per unit change in elevation are greatest (Figure 2). However, about 30% of all the high tides inundated all of the ditched sites. In contrast, most thresholds for the natural sites correspond to positions above the MHHW tidal plane, where tidal inundation is relatively infrequent and short in duration (Figure 2, Table 1).
Aquatic macroinvertebrate
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TABLE 1. Characteristics of the tidal regimens of the main ditched (Dl-D3), natural (Nl-N3), and highest threshold (HS) study sites, based upon continuous measurements for the duration of the sampling year (April 1980 to March 1981)
Site
Threshold to MHHW
Dl D2 D3 Nl N2 N3 HS
relative (cm)
-15 - 14 -5 0 f10 f15 f20
No. of inundations per year 328 318 261 210 98 56 41
main tidal
Total hours of inundation per year 1170 1090 780 605 245 110 70
All of our study sites supported floating, aquatic vegetation, at least during part of our sampling year. This cover was dominated by green algae, including Enteromorpha cZathrata (Roth) Grev., Ulothrix j&zcca (Dillw.) Thur., and Ulva sp. Some sites also supported small amounts of widgeon grass, Ruppia maritima L., which was the only macrophyte among our study sites. Environmental
data
Preliminary field work was begun in November 1979; quantitative data were collected from April 1980 to March 1981. Water salinity within each study site was measured weekly with a refractometer. Weekly values for the duration and frequency of tidal immdation were derived from the continuous record of the tide gauge. Visual estimatesof the percent aquatic plant cover at each main site were made weekly. In situ max/min thermometers were used to measure weekly temperature extremes at the main sites. In the summer of 1980, thermographs were installed at two adjacent potholes, one ditched and one natural, to determine the effects of tidal inundation on pothole temperature. The thermographs were used over a complete lunar cycle (10 August to 10 September 1980). Biological
data
During the year of data collection, three 180-cm2 sampleswere taken monthly at each main site. On two of the twelve sampling dates, sampleswere taken at high tide; at all other times samples were taken during slack low tide. All samples were taken at the centers of randomly selectedquadrats, and no quadrat was selectedmore than once. In sampling, a l-m long, 15.25-cm diameter PVC pipe was thrust 5 cm into the pothole substrate, then removed by covering the pipe bottom and lifting upward. Since we had established that the bottom 4 cm of a sample were composed of anoxic substrate that contained no living organisms, only the water and the uppermost 1 cm of substrate were retained for processing. Each sample was washed consecutively through sieveswith 2 mm (no. lo), 1 mm (no. 18), and 500 p (no. 35) pore sizes. The washed material was then floated on saturated salt solution to facilitate the sorting of specimens.The biomassof a samplewas determined by oven-drying to constant weight at 105 “C; prior to weighing, sampleswere cooled with dehydrated air. Analysis
Simple linear regression was used to measure how each environmental factor varied along the inundation threshold gradient. We used two-way analysis of variance to test
336
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30 . G < 0 h'
A. Barnby,J.
(0)
i 25 -
& V. H. Resh
.
.*
(bi
2
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l \_.
I
.
l
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l
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1’ DI D2 -15 -14
1 D3 -5
I NI 0
I N2 t10 Site
1 N3 t15
lnundatlon
I HS t20 threshold
I II DI D2 -15 -14 relative
I 02 -5
I NI 0
to MHHW
(cm)
I N2 HO
I N3 fl5
I HS t20
Figure 3. Relationships between inundation threshold and weekly temperature range for (a) wet and (b) dry seasons. For the wet season, dashed line represents weeks with at least 1.25 cm rainfall; solid line represents weeks with less rainfall.
the hypotheses that neither seasonal biomass nor species diversity (Simpson’s Index, sensu Routledge, 1979) differed between the ditched and the natural potholes. Linear discriminant analysis (Klecka, 1975) was used to measure the similarity of physical conditions and fauna1 composition among the main sites, and to determine if any species assemblages were indicative of particular inundation thresholds or pothole conditions. Discriminant analysis reduced each data case (i.e. a set of date- and sitespecific measurements of physical parameters or population densities) to a single summary index (i.e. the discriminant score). Each case was then reassigned, according to its score, to one of the six main sites, with the discriminant functions minimizing the probability of incorrectly reassigning data. The absolute magnitudes of the discriminant function coefficients, which weight each variable in a case, were used to identify the species or physical parameters that were most important for correctly classifying cases. The mean discriminant score (i.e. the centroid) for each site was plotted, using the discriminant functions to calculate Cartesian coordinates. Physical and fauna1 similarities among the sites were then inferred from the relative positions of the centroids. Results The
and discussion
environment
of a pothole
The physical data indicate that the environment of a pothole varies according to its inundation threshold. For example, weekly pothole temperature range descreased with increasing threshold for the wet and dry seasons [Figure 3(a), (b), respectively]. This is because temperatures in ditched potholes are regularly influenced by the tides, which both import and export heat. Night-time flood tides, which in general are warm relative to the soil and air, and the relatively cool daytime flood tides exchange less heat with the air and soil while traveling through a full ditch than when traveling as a thin sheet of water over the marsh surface (Felton, 1978). As a result, temperature differences between water already in a pothole and the incoming tidal water are greater for the
Aquatic
macroinvertebrate
337
communities
(b)
I
Site
lnundotlon
threshold
II DI D2 -15 -14
relatwe
I D2 -5 to MHHW
1 NI 0
I N2 +I0
I N3 t15
I HS +20
(cm)
Figure 4. Relationships between inundation threshold and variability of temperature range for (a) wet and (b) dry seasons. Variability is reported as the monthly coefficient of variation calculated from weekly temperature ranges.
ditched than the natural study sites. Also, when tides recede from the marsh surface, ditched potholes are nearly drained, and the remaining shallow water rapidly exchanges heat with the atmosphere. Thus, both frequent inundation and changes in water level can cause ditched potholes to have broad temperature ranges during short (i.e. 1 week) time periods. When longer periods of time (i.e. 1 month) were considered, the variability of weekly temperature range was positively correlated with inundation threshold for both the wet and dry seasons [Figure 4(a), (b), respectively]. This is because regular inundation reduces the influence of atmospheric temperatures, which vary more than the temperatures of the tides. Among all the study sites, salinity was lower and more uniform in the wet season than in the dry season [Figure 5(a), (b)], b ecause wintertime increases in rainfall and river discharge reduced salinities throughout the marsh. During the dry season, the more frequent tidal flushing in ditched potholes generally prevented salt accumulation, whereas in natural potholes low rates of flushing allowed salts to concentrate. Among potholes with similar tidal regimens, those covered with thick algal mats had higher salinities than those lacking such cover. For example, the scant algal cover in pothole Nl [Figure 6(a)] was probably responsible for its low salinities relative to D3, a site which had a slightly lower inundation threshold but much greater algal cover [Figure 6(b)]. Since a filamentous algal mat increases pothole surface area, the mat can also increase evaporative water loss, and thus increase pothole salinity. At Petaluma Marsh, evaporative losses due to algal mats might be accelerated by afternoon winds that reduce the water vapor pressure at the marsh surface. This influence of algae on salinity may be responsible for the low, but significant positive correlation between inundation threshold and weekly maximum salinity for the dry season (r=0.25; P
338
M.
A. Barnby,J.
N. Collins
Q
V. H. Resh
(a) 140
Figure highest
1
I I I I I I I I Nov JUI Sep May 5. Seasonal patterns of change in salinity threshold sites (HS), and (b) ditched study
II Jar
11 I
Mar
for (a) natural sites.
sites including
the
tidal regimen, algal cover, evaporation, and precipitation caused fluctuations in pool salinities in a salt marsh located near the Bay of Fundy, Nova Scotia. In contrast, Ward & FitzGerald (1983~) found that temperature in a Quebec salt marsh was the major factor controlling pool salinities, although algal cover did not differ among the pools they studied. Percent algal cover was positively correlated with inundation threshold, especially in the dry season (r = 0.60; P < 0.0 1). However, algal cover was highly variable, even among study sites with similar thresholds. Although our data do not indicate reasons for the variable distribution of algae among the natural sites, some mechanisms for cover reduction at potholes with low thresholds can be inferred. For example, relatively high frequencies of tidal flushing may have disrupted the algal mats and caused their export. A similar mechanism was suggested for the lack of an established algal cover in a low elevation pool in a Quebec salt marsh (Ward & FitzGerald, 1983~). Our analysis of abiotic parameters suggests that high threshold potholes are environmentally severe habitats for macroinvertebrates. In potholes with high
Aquatic
100 75
macroinvertebrate
339
communities
I (0) -
N2
-
./;)
. .
. . .
. . .
. . . .
(ijL1.l-.-
..a.=
. --. . .
. . . .
. -‘-.-
(.T)
50
8 ‘= IFi
(b) 100
-
JlJn
May
Figure sites.
6. Percent
algal cover
Sep of water
Nov
surface
Jan
for (a) natural
Mar
and (b) ditched
TABLE 2. Mean values* S.D. of total macroinvertebrate community for natural and ditched potholes in the wet and dry seasons
Natural Wet season Dry season
0.061+ 0.045
main study
biomass
(gm-‘)
Ditched 0.041
& 0.045
0,056 0.043
k 0.043 k 0,032
thresholds, infrequent tidal inundation can result in very high salinities and habitat desiccation. Although temperatures can be extreme for low threshold potholes, thermal regimens are more variable for potholes with high thresholds. Therefore, any aquatic macroinvertebrate populations living in high threshold potholes will be subject to environmental conditions that involve very high salinities, insufficient moisture, and irregular and unpredictable changes. Community
parameters
Biomass
Wet season community biomass was significantly higher than dry season biomass (P = 0.05) in both the natural and ditched sites, whereas differences in biomassbetween ditched and natural sites were not significant for either season(P=O.71; Table 2). The higher invertebrate biomass during the wet seasonmay have resulted from increased food resources. For example, we observed that most algal mats began decomposing in early winter, when detritivores dominated the pothole fauna. Similarly, Cameron (1972) reported that organic debris increased during wintertime in a nearby salt marsh, and this
340
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N. Collins & V. H. Resh
material provided a large food source for invertebrate detritivores. We alsoobserved that macroinvertebrates did not feed on viable algal mats, and infer that the healthy algal mats that occurred during summer were more important asmicrohabitat than as food. Species richness
The species richness of the aquatic macroinvertebrate fauna of Petaluma Marsh is apparently higher than that reported for other salt marshes. Nicol (1935) collected 13 species of insects in an English salt marsh; Campbell & Denno (1978) collected 20 speciesof insects in a New Jersey salt marsh; Kelts (1979) collected 19 speciesof insects in a New Hampshire salt marsh; and Ward & FitzGerald (1983~) collected 12 speciesof insects in a Quebec salt marsh. At Petaluma Marsh we collected 60 166 specimens representing 32 taxa of macroinvertebrates, of which 24 taxa were insects (Table 3). However, results from these studies are not strictly comparable, since different sampling methods were used. Our study also revealed a much richer insect fauna for Petaluma Marsh than previously described by Greenstone (1978), but he did not actually sample the pothole invertebrates. In addition, the collection of 8322 insect specimens that comprised 18 taxa from our three ditched study sites disagrees with the assertion by Greenstone (1983) that ditched potholes in Petaluma Marsh are devoid of aquatic insects. Speciesrichness was always higher for sitesNl through N3 than for either the ditched or the highest elevation sites (Figure 7). This pattern may be a function of changes in either the disturbance rate or habitat severity along the inundation threshold gradient. Among low threshold potholes, tidal disturbances (i.e. sediment transport, algal export, and changesin water level, salinity, and temperature) are frequent, whereas severe conditions (i.e. very high salinities and desiccation) are most probable among potholes with the highest thresholds. According to the ‘ Intermediate Disturbance Hypothesis ’ (Connell, 1978), speciesrichness is greatest where rates of habitat disturbance or habitat severity are intermediate. In our study, plots of richness versus inundation threshold for both the wet and dry seasons[Figure 8(a), (b)] resemble the relationship predicted by Connell (1978). Other studies have shown that marine invertebrate speciesdiversity is greatest where disturbance rates are not extreme (e.g. Levin & Paine, 1974; Sousa, 1979). Species diversity
During both the wet and dry seasons,speciesdiversity was significantly higher for the natural than the ditched potholes (P < 0.01); however, no significant seasonaldifferences were found (P=O.81; Table 4). The patterns of speciesdiversity among our study sites reflected differences in abundances of the most common taxa, which corresponded to environmental differences along the threshold gradient. For example, the density of the most common invertebrate, the oligochaete Paranais litoralis (Miiller) (Figure 9), was both directly and indirectly influenced by environmental factors. In potholes Dl and D2, the amount of filamentous algaewas insufficient to serve asrefuge for P. litoralis. As a result, P. 1itoraZis was probably consumed in large numbers by the secondmost common macroinvertebrate, the water boatman T. reticulata, which is at least a facultative consumer of small animals (Carpelan, 1957; Davis, 1966; Cox, 1969). In potholes D3 and Nl, however, large numbers of P. litoralis were probably able to avoid predation by inhabiting filamentous algae. This conclusion is based on repeated observations that algal mats typically contained large numbers of P. litoralis, whereas nymphs and adults
Aquatic
macroinvertebrate
341
communities
3. Fauna collected at all study sites during wet and dry seasons in Petaluma Salt Marsh. For the natural and ditched main sites, counts are totals per season. Only presence (+) or absence of species is indicated for the highest threshold sites
TABLE
Natural wet Polychaeta
sp.
Oligocheata Lumbriculus lineatus Miiller Paranais litoralis (Miiller) (these counts include Tubijicoides nethoides (Brinkhurst) and two undescribed species of Rhyacodrilinae, all of which are rare taxa in samples)
Ditched wet
dry
8 55 11192
Highest dry
wet
13
6
113 12 7287 20716
58 5982
23
Crustacea Tanais vanis Miller Anisogammarus confer&ohs (Stimpson)
12
5
23
5
1552
196
198
35
Insecta Hemiptera Trichocorixa reticulara (Guerin-Meneville)
867
1957
1201
5859
Diptera Chironomus sp. Cricotopus sp. Hydrobaenus sp. Dasyhela sp. Psychoda salicornia Quate Aedes dorsalis (Meigen) Aedes squamiger (Coquillett) Dolichopus sp. Eristalis tenax Linnaeus Tabanus laticeps Hine Odontomyia sp. Chiromyzinae sp. Ephydra millbrae Jones Lamproscatella muria Matis Scatella stagnalis Fallen Paracoenia bisetosa (Coquillett) Hydrellia griseola (Fallen) Canace sp. Cyclorrhapha sp.
83 101 3 43 3 4 2 35 9 0 41 1 242 32 0 0 1 0 5
0 0 0 21 2 0 0 95 6 0 16 1 344 16 1 0 1 1 3
0 8 1 73 252 0 0 45 1 0 4 2 253 5 1 3 0 40 1
0 0 3 21 138 0 0 34 1 1 1 0 223 19 0 0 0 3 0
Coleoptera Enochrus diffusus (Le Conte) Berosuspunctatissimus Le Conte Tropisternus salsamentus Fall Ochthebius rectus Le Conte
236 16 0 13
147 0 3 2
87 0 0 3
39 0 0 0
dry
+
+ +
+
of T. reticulata were never observed within these mats. Among potholes with higher thresholds, harsh conditions (i.e. high salinity and frequent desiccation) may have directly limited the density of P. litoralis. For example, low numbers of P. litoralis were sampled in pothole N3, although filamentous algae were abundant and T. reticulata was scarce.
342
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HS ---->
2-
1
0-N I
w
I
&
V. H. Resh
,-
b----c----
I JUl
I
I Sep
I
I Nov
I
‘\-’ I JCUl
Figure 7. Temporal patterns of species richness study sites and highest threshold sites (HS).
fj-
I
I Mar
for ditched
(D) and natural
(N)
main
(0) -
6-
I
4-
2-
I
I I DI 02
I D3
I NI
I N2
I N3
I HS
Figure 8. Relationship between species richness and environmental severity or rate of habitat disturbance as represented by inundation threshold (i.e. relative positions along the abscissa reflect height above MHHW) for (a) wet and (b) dry seasons. Means and error bars for the highest threshold sites are based upon weekly collections. TABLE 4. Mean values& 1 S.D. of total macroinvertebrate community diversity (Simpson’s index) for natural and ditched potholes in the wet and dry seasons Natural Wet season Dry season
1.04+051 1.12kO.59
Ditched 0,70+0.32 0,66*0.37
Aquatic macroinvertebrate
$ I :::;I May Jul
Figure
Sep
Nov
communities
Jon
Mar
343
May JUI
Se0
Nov
9. Temporal patterns of the abundance (log,,) of P. litoralis reticulata( W -- n ), and A. confervicolus (A A), at the main study sites are represented by graphs (a)-(c); ditched sites by graphs (d)-(0.
Jan
Mar
(O-a), T. sites. Natural
Two environmental factors probably allowed populations of T. reticulata to attain very high densities, such as those which occurred in the two lowest threshold ditched sites and in the lowest threshold natural site (i.e. Dl, D2, Nl; Figure 9). First, frequent inundation reduced the risk of habitat desiccation and the consequential stranding of immature, wingless water boatmen (Balling & Resh, 1984). Second, since these three potholes contained relatively small amounts of floating algal cover [Figure 6(a), (b)], they were probably more intensively colonized by aerial adult water boatmen. This is because adults that alight on algae tend to explore it briefly, then take flight, whereas those that land in open water tend to remain. Increased water salinities were apparenty not a factor in reducing the numbers of T. reticulata in potholes with high inundation thresholds, since dense populations have been observed in high threshold potholes that were devoid of algal cover and where water salinities were two to four times asconcentrated as seawater. Also, Carpelan (1957) found the highest population densities of this species in very saline (i.e. 63%0) salt evaporation ponds located adjacent to southern San Francisco Bay. The spatial and temporal occurrence of the third most common invertebrate, the amphipod Anisogammarus confervicolus (Stimpson) (Figure 9), might also have been directly affected by conditions of algal cover. That is, populations of A. confervicolus were most abundant during the wet season, and were essentially restricted to high threshold potholes containing large amounts of deteriorating filamentous algae. Since A. confervicolus is a detritivore, the decomposing algal mats probably served as a food resource. A similar relationship between occurrence of A. confervicolus and filamentous algae was observed by Carpelan (1957) in salt evaporation ponds near southern San Francisco Bay. In the above discussion, we suggestthat many of the differences in macroinvertebrate community structure that we observed among potholes in Petaluma Marsh were due to differences in abiotic factors and algal cover. This is in contrast to Campbell & Denno (1978), who ascribed spatial differences in invertebrate community structure among unditched potholes in a New Jersey salt marsh to predation by birds and fish. However,
M. A. Barnby,J.
344
N. Collins & V. H. Resh
(a) NI .
NI .
DI . .
D2
l
N3 .
.
N2
D3
.
D3 .
Monthly
lnundatlon
frequency
Figure 10. Plots of (a) wet and (b) dry season main site discriminations based upon environmental parameters. Each site is represented by its centroid (see methods). The most discriminating factors of the first and the second functions are given as labels for the abscissa and ordinate, respectively. Distances among centroids parallel to either axis indicate absolute differences; the axes do not indicate direction of increase or decrease in paremeter value.
these salt marsh pools may be less variable as habitats, and therefore might support invertebrate communities that are lessregulated by physical factors than the communities in Petaluma Marsh. Signs of bird visitation were rare among our study sites, and we infer that predation by birds generally did not influence the structure of the macroinvertebrate communities. Furthermore, at Petaluma Marsh the invasion of potholes by large numbers of fish was apparenty both spatially and temporally uncommon, and probably did not affect macroinvertebrate community structure. In fact, we observed fewer than 50 fish among our study sites during more than 150h of reconnaissancespanning 12 consecutive months. Almost all of these fish were threespine stickleback, Gasterosteus aculeatus L., which apparently only invade potholes during tidal inundation and feed almost exclusively on microcrustacea (Balling, unpublished data). In addition, caged experiments in a salt marsh pool in Quebec indicated that G. aculeatus had no measurable impact on the macroinvertebrate community (Ward & FitzGerald, 1983b). Environmental
and fauna1 similarity
The environment
Based upon environmental factors, the discriminant functions correctly classified 89U,, and 86% of the data casesfor the wet and the dry seasons,respectively. This indicates successful classification relative to the 16y; chance (1 in 6) of randomly assigning the data casesto the correct study sites. Incorrect classification of casesoccurred mainly among potholes with similar inundation thresholds. The discriminant analysis basedupon environmental factors indicated that each main site was environmentally unique, but that those sites that have the most similar inundation thresholds were also most similar with regard to temperature, tidal regimen, salinity, and percent plant cover. For example, although the percent correct classification was always high, the centroids for potholes Dl and D2 were consistently plotted together, as were centroids for potholes N2 and N3 [Figures 10(a), (b)]. Although the centroids for the two sites with intermediate thresholds (i.e. D3, Nl) were plotted apart from one another, they were consistently plotted between the centroids for the higher and lower threshold sites. These four sites (i.e. Dl, D2, N2, N3) were primarily distinguished by differences in inundation threshold, whereas the sites with intermediate
Aquatic
communities
macroinvertebrate
(0)
345
(b)
N3
Nl . . D2 l
N3 .
03
l
.D3 N2 .
61
DI ’
b2
r;l r;2 Monthly
density E. DlffUWS
of
Monthly Doltchopus
density of and E. teenox
Figure 11. Plots of (a) wet and (b) dry season main site discriminations based upon fauna1 composition and species density. Each site is represented by its centroid (see methods). The more important taxa of the first and second discriminating functions are given as labels for the abscissa and ordinate, respectively. Note that the axes only show absolute differences; the direction of increase or decrease in species density is not indicated.
thresholds (i.e. D3, Nl) were distinguished mainly by differences in salinity [Figures 10(a), (b)]. The pattern of classification for sitesD3 and Nl probably reflects the higher salinities causedby the greater algal cover in site D3 relative to site Nl. The fauna
If the macroinvertebrate species assemblagesof potholes are indicative of discrete positions along the inundation threshold gradient, then the study sites can be classified according to their fauna1characteristics, and the pattern of classification (i.e. the relative positions of the centroids in the discriminant function plots) should resemble that based upon the environmental features. Using population densities of all speciesas variables, 72:/b and 67% of the caseswere classified correctly for the wet and dry seasons,respectively. Again, this indicates successful classification relative to the 16:& chance (1 in 6) of randomly assigning data cases to the correct study sites. Also, the centroids for the sites generally were plotted according to their position along the threshold gradient [Figure 1l(a), (b)]. For both seasons, the centroids for the ditched potholes were grouped together and the centroid for the next higher pothole (i.e. Nl) was plotted nearby. The centroids for the two siteswith the highest thresholds (i.e. N2, N3) were plotted apart from each other and the rest. These results indicate that ditched and natural potholes with different inundation thresholds below MHHW (e.g. Dl-Nl) support similar macroinvertebrate faunas, whereas potholes with different thresholds above MHHW (e.g. N2, N3) support faunas that are more distinct. Furthermore, since physical conditions were similar for potholes N2 and N3 [i.e. basedupon physical factor centroids; Figure 10(a), (b)], the distinctiveness of their faunas suggests that slight differences in threshold (e.g. 5 cm) above MHHW can result in relatively large differences in speciescomposition and population density. Rare taxa, found primarily at sites Nl-N3, were important in distinguishing these sites from the ditched sites. For the wet season[Figure 1l(a)], the most important discriminators were Enochrus difluusus(Le Conte) larvae and adults, and larvae of the chironomid genera Cricotopus and Chironomus. For the dry season[Figure II(b)], the most important taxa were Dolichopus larvae, larvae of the rat-tailed maggot Eristalis tenax L., and larvae of E. diffusus.
346
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N. Collins
Q
V. H. Resh
Conclusions Although the surface of Petaluma Marsh approximately corresponds to the mean height of the higher high tides (MHHW), an elevational gradient from at least 15 cm below MHHW to 20 cm above the tidal datum is represented by the inundation thresholds of potholes. Both the frequency and duration of tidal inundation among salt marsh lentic environments decrease exponentially with linear increases in inundation threshold. However, habitat conditions are most variable among potholes with intermediate thresholds that approximately correspond to MHHW, where slight differences in threshold can result in ecologically significant differences in salinity and moisture. In Petaluma Marsh, macroinvertebrate community structure and fauna1 composition vary among potholes according to differences in habitat conditions, which are regulated by the tides. For a given season, species richness is lowest and fauna1 composition is most similar among potholes that have very high (i.e. > 15 cm above MHHW) inundation thresholds, and therefore have environmental conditions that tend to be extreme. Among potholes with very low thresholds (i.e. < 10 cm below MHHW), habitat conditions are relatively simple, invariant, and not severe; consequently, species richness and diversity are relatively low, and fauna1 composition is similar throughout the year. Among potholes with intermediate thresholds (i.e. near MHHW), significant differences in habitat conditions correspond to slight differences in threshold. Fauna1 composition is most variable among these potholes, and species richness and diversity are relatively high. When a pothole is ditched, its inundation threshold is lowered, usually from an intermediate position near MHHW, to a new position much below that tidal datum. Consequently, its environmental characteristics and the macroinvertebrate community that it supports becomes less complex and more indicative of a broad range of lower elevation tidal regimens. Since ditched potholes are more numerous than ponds and natural potholes combined, a large proportion of the lentic habitats in Petaluma Marsh probably support macroinvertebrate communities that are now simpler and more alike one another than they were prior to ditching. Acknowledgements We thank S. S. Balling for project assistance and R. 0. Brinkhurst for oligocheate identifications. Support for this project was provided by University of California Mosquito Research Funds. References Atwater, B. F., Conrad, S. G., Dowden, J. N., Hedel, C. W., MacDonald, R. L. & Savage, W. 1979 History, landforms and vegetation of the estuary’s tidal marshes, pp. 347-385. In San Francisco Bay: The Urbanized Esruarv (Conomos, T. T., ed). Pacific Division, American Association for the Advancement of Science, San Francisco, 493 pp.Balling, S. S. & Resh, V. H. 1982 Arthropod community responses to mosquito control recirculation ditches in San Francisco Bay salt marshes. Environmental Entomology 11,801-808. Balling, S. S. & Resh, V. H. 1983 The influence of mosquito control recirculation ditches on plant biomass, production, and composition in two San Francisco Bay salt marshes. Estuarine Coastal and Shelf Science 16, 151-161. Balling, S. S. & Resh, V. H. 1984 Life history variability in the water boatman Trichocorixa reticulara (Hemiptera: Corixidae) in San Francisco Bay salt marsh ponds. Annals of the Entomological Society of America 17,14-19.
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Balling, S. S., Sroehr, T. & Resh, V. H. 1980 The effects of mosquito control recirculation ditches on the fish community of a San Francisco salt marsh. California Fish and Game 66,25-34. Bamby, M. A. & Resh, V. H. 1980 Distribution of arthropod populations in relation to mosquito control recirculation ditches and natural channels in the Petaluma Salt Marsh of San Francisco Bay. Proceedings of the California Mosquito and Vector Control Association 48,100-102. Bleakney, J. S. & Meyer, K. B. 1979 Observations on saltmarsh pools, Minas Basin, Nova Scotia, 1965-1977. Proceedings of the Nova Scotia Institute of Science 29,353-371. Cameron, G. N. 1972 Analysis of insect trophic diversity in two salt marsh communities. Ecology 53,58-73. Campbell, B. C. & Denno, R. F. 1978 The structure of the aquatic insect community associated with intertidal pools on a New Jersey salt marsh. Ecological Entomology 3,181-187. Carpelan, L. H. 1957 Hydrobiology of the Alviso salt ponds. Ecology 38,375-390. Collins, J. N. & Resh, V. H. 1985 Utilization of natural and man-made habitats by the salt marsh song sparrow, Melospiza melodiu samuelis Baird. California Fish and Game (in press). Connell, J. H. 1978 Diversity in tropical ram forests and coral reefs. Science 199,1302-1310. Connell, W. D. 1940 Tidal inundation as a factor limiting the distribution of Aedes spp. in a Delaware salt marsh. Proceedings of the New Jersey Mosquito Extermination Association 27, 166-177. Cox, M. C. 1969 The biology of the euryhaline water boatman Trichocorixa reticulata (Guerin-Meneville) (Hemiptera-Corixidae). M.S. Thesis, California State University, San Diego. 84 pp. Davis, C. C. 1966 Notes on the ecology and reproduction of Trichocorixa reticulum in a Jamaican salt-water pool. Ecology 47,850-852. Felton, C. R. M. 1978 The energy budget of a south San Francisco tidal salt marsh. Ph.D. thesis, University of California, Berkeley, California. 322 pp. Greenstone, M. H. 1978 The numerical response to prey availability of Purdosa ramulosa (McCook) (Araneae: Lycosidae) and its relationship to the role of spiders in the balance of nature. Symposia of the Zoological Society of London 42, 183-193. Greenstone, M. H. 1983 Site-specificity and site tenacity in a wolf spider: A serological dietary analysis. Oecologia S&79-83. Hinde, H. P. 1954 Vertical distribution of salt marsh phanerograms in relation to tide levels. Ecological Monographs 24,209-225. Kelts, L. J. 1979 Ecology of a tidal marsh corixid, Trichocorixa verticalis (Insecta, Hemiptera). Hydrobiologia 64,37-57. Klecka, W. R. 1975 Discriminant analysis. pp. 434-467. In SASS, Statistica Package for the Social Sciences. Nie, N. H., Hull, C. H., Jenkins, J. G., Steinbrenner, J. and Bent, D. H. (eds). 2nd ed., McGraw-Hill Book Co., New York, 675 pp. Levin, S. A. & Paine, R. T. 1974 Disturbance, patch formation and community structure. Proceedings of the National Academy of Science (U.S.A.) II, 2744-7. Marmer, H. A. 1951 Tidal Datum Planes. Special publication no. 135, U.S. Dept. Commerce, U.S. Government Printing Office, Washington, D.C. 142 pp. Nicol, E. A. T. 1935 The ecology of a salt-marsh. Journal oj the Marine Biological Association of the United Kingdom 20,203-26 1. Resh, V. H. & Balling, S. S. 1983~ Ecological impact of mosquito control recirculation ditches on San Francisco Bay marshlands: Study conclusions and recommendations. Proceedings of the Cultfornia Mosquito and Vector Control Association 51,49-53. Resh, V. H. & Balling, S. S. 19836 Tidal circulation alteration for salt marsh mosquito control. EnvironmentaZ Management 7,79-84. Routledge, R. D. 1979 Diversity indices: Which ones are admissible? Journal of Theoretical Biology 76, 503-515. Smith, J. B. 1904 The common mosquitoes of New Jersey. Bulletin of the New York AgricuZturaZ Experiment Station 171, l-40. Sousa, W. P. 1979 Disturbance in marine intertidal boulder fields: the nonequilibrium maintenance of species diversity. Ecology 60, 1225-1239. Ward. G. & FitzGerald. G. 1. 1983a Macrobenthic abundance and distribution in tidal ~001s of a Quebec salt marsh. Canadi&3ournaZof Zoology 61, 1071-1085. Ward, G. & FitzGerald, G. J. 19836 Fish predation on the macrobenthos of tidal salt marsh pools. Canadian 3ournaZof Zoology 61, 1358-1361. Yapp, R. H., Johns, D. & Jones, 0. T. 1917 The salt marshes of the Dovey Estuary. Part II. The salt marshes.Journal of Ecology $65-103.