Long term effects of climate on two pond predators.
Abstract: This study assessed the influence of annual snowpack on long term changes in the predatory regime of four high elevation ponds in the mountains of northwest Wyoming. Over 36 y of observation, in two ponds the primary predator alternated between phantom midge Chaoborus americanus larvae and Diaptomus shoshone predatory copepods, whereas the predatory regime did not change in the other two shallower ponds. Switching of predators correlated with extreme amounts of winter snow, either high or low, which determined the depth at which drying or complete freezing of the pond occurred. Chaoborus americanus colonized ponds after the wettest years and disappeared after the driest years. The results provide an unusual long term perspective of the effects of weather on predator dominance.
Article Type: Report
Subject: Climatic changes (Environmental aspects)
Predation (Biology) (Environmental aspects)
Ponds (Environmental aspects)
Author: Williams, Ernest H.
Pub Date: 04/01/2012
Publication: Name: The American Midland Naturalist Publisher: University of Notre Dame, Department of Biological Sciences Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Earth sciences Copyright: COPYRIGHT 2012 University of Notre Dame, Department of Biological Sciences ISSN: 0003-0031
Issue: Date: April, 2012 Source Volume: 167 Source Issue: 2
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 287956854
Full Text: INTRODUCTION

Responses of freshwater communities to the effects of vertebrate and invertebrate predators can be extensive and complex (Brooks & Dodson, 1965; Lynch, 1979; Kerfoot & Sih, 1987; Black & Hairston, 1988; Riessen et al., 1988; Hanazato & Yasuno, 1989; Brett & Goldman, 1996). Phantom midge larvae (Chaoborus spp.) are important invertebrate predators in many lake and pond communities, feeding on rotifers, cladocera, and copepods (Elser et al., 1987; Luecke, 1988) and exerting varying effects on different zooplankton species (MacKay et al., 1990). Another group of invertebrate predators, large diaptomid copepods, also affect coexisting cladocera and copepods wherever they are found (O'Brien, 2001), even though these copepods may not be obligate predators (Kling et al., 1992). One such species, Diaptomus shoshone Forbes, is widespread in alpine and subalpine lakes of western North America (Anderson, 1971; Stoddard, 1987; Larson et al., 2009) and predaceous on crustacean zooplankton (Anderson, 1967; Williams, 1980). Large diaptomids like these exert strong effects on the communities of high elevation oligotrophic bodies of water, where food webs are usually simple (Hebert & Hann, 1986; Paul et al., 1995; O'Brien, 2001).

A study by Williams (1976) of the zooplankton in lakes and ponds of the Beartooth Mountains, WY, revealed several distinct communities, each associated with one primary predator and with the distribution of predators determined primarily by physical characteristics of the water body. Planktivorous Chaoborus americanus (Johannsen) larvae were found in fishless pothole ponds (see Kurek et al., 2010) with soft bottoms and extensive growth of sedges around the margins, and the copepod Diaptomus shoshone was found in shallow, hard-bottomed ponds. Fourth instar C. americanus fed heavily on D. shoshone in soft-bottomed pothole ponds (Williams, 1976, 1980), and D. shoshone adults fed on first instar C americanus; consequently, the predators displayed a disjunct distribution (Williams, 1980). Chaoborus americanus have been found by others as well to significantly reduce the abundance of diaptomid copepods (MacKay et al., 1990), though 1ess has been reported about reciprocal predation.

Several ponds in the original study were marginal in the physical characteristics of typical Chaoborus americanus ponds, and midge larvae occurred in them in some years but not in others (Williams, 1976). To assess the influence of weather on changes in the predatory regime, I continued sampling two pairs of ponds for predator shifts over the next 36 y. I expected to find that heavy snowpack would increase water depth and make a pothole pond more suitable for C. americanus, which must overwinter as larvae, while low snow pack would decrease water depth and make a marginal pond more likely for dominance by Diaptomus shoshone, which overwinter as encysted eggs. Thus, winter weather, a factor external to the community, would determine the form of the predatory regime.

MATERIALS AND METHODS

Ponds in the Beartooth high lakes district of northwest Wyoming (Table 1) were sampled in mid to late summer from 1974 through 2009. These four ponds occur as pairs in close proximity; one pond of each pair was shallower with a harder bottom, so it could be compared to the other with a softer bottom. All sampling over the 36 y was done using the same procedures and by the same person, so despite the length of time, the techniques were consistent from the first to the last sampling. A few years were missed during this 36 y span, so the number of years actually sampled ranged from 29 to 32, depending on the pond (Table 1). The location of each pond was calculated using Google Earth (Google Earth, 2010), and surface areas were determined from ImageJ (Rasband, 2009) analysis of Google Earth images. In the first years of the study, the depth of each pond was measured on each sampling date directly by meter stick in the deepest area.

The invertebrate predators Diaptomus shoshone and Chaoborus americanus were sampled with a 15.2 cm diameter conical townet with #20 fine nylon monofilament mesh. Each pond was sampled by making horizontal throws with the net at the end of a calibrated 10 m line and recording the actual length of the tow to the nearest half meter. Generally the samples from three different throws were combined. Occasionally, a pond was too shallow to obtain a quantitative sample, so the net was hauled quickly near the surface to obtain a nonquantitative sample. Samples were preserved by adding 95% ethyl alcohol in the field and then later transferring the contents to 70% ethyl alcohol with glycerin. Numbers of D. shoshone and C. americanus were counted from each sample under a Nikon SMZ-10 dissecting microscope at 15x magnification. The species were identified in the original study (Williams, 1976) using Wilson & Yeatman (1959) for D. shoshone and Johannsen (1934) and Saether (1970) for C. americanus.

Because the filtration efficiency of plankton nets (the volume of water actually filtered compared to the calculated volume) depends on the design of the net as well as how it is used (Tranter & Smith, 1968; McQueen & Yan, 1993), the percent efficiency of the net used in this study was determined with a General Oceanics Digital Flowmeter, model 2030, with both R and R6 (low speed) rotors. To determine the net's efficiency, the field sampling techniques were mimicked in an indoor swimming pool by making tows with the meter both inside and outside the net. The counts on the flowmeter recorded from 10 tows inside and 10 outside (comparison of counts from the two locations: [t.sub.18] = 12.094, P < 0.001) yielded an efficiency of 58.9% (95% CI = 54.8% to 63.1%). All calculated densities of Diaptomus shoshone and Chaoborus americanus were adjusted accordingly.

Records of snow pack (SNOTEL data as water equivalence) were obtained from the NRCS National Water and Climate Center (NRCS, 2010) for the Beartooth Lake pillow (site 326), which reports data from 1981 on. The study ponds are less than 4 km from this recording station. Statistical analysis was with PASW Statistics 19 (SPSS, 2010), using independent samples t-test for comparisons, univariate general linear model (ANOVA) for analysis of the aggregated data, and regression analysis to examine the reciprocal densities of the two predators.

RESULTS

The original survey (Williams, 1976) showed pond G2 to be intermediate in depth and softness between characteristic soft-bottomed Chaoborus americanus and hard-bottomed Diaptomus shoshone ponds, and D. shoshone and C. americanus dominated communities have occurred in this pond as alternative states during the 36 y study period. From 1974 through 1988, C. americanus was the only predator in G2, in densities from 0.01-1.41/L; in contrast, D. shoshone was abundant from 1989 through 1997, at densities from 0.13-1.07/L, with a single chaoborid found in the samples during these 9 y (Fig. 1). The community switched back to C. americanus dominance from 1998 through 2009, with densities up to 1.41/L. However, when C. americanus declined in 2002 and 2004 to its lowest abundance, D. shoshone reappeared (Fig. 1). Snowpack was not significantly different when comparing the sets of years in which each predator was dominant ([t.sub.20] = 1.087, n.s.), but the changes in predatory regime occurred after years of snowpack extremes. The switch to D. shoshone occurred after the low snowfall year of 1987 (2.5 cm, the lowest depth recorded on May 15 during 19812009), and D. shoshone reappeared in the pond after the low snowfall year of 2001 (22.4 cm, the second lowest amount recorded for 1981-2009). The change towards C. americanus dominance took place after the heavy snowpack years of 1996 and 1997 (99.6 and 87.6 cm; during the same 1981-2009 period, these were the 2 y with the deepest snow). In comparing extreme conditions, there are too few replicates for statistical analysis, but the differences were dramatic: the lowest snowpack values correlated with a shift to D. shoshone, whereas the highest recorded values correlated with the shift to C. americanus.

Pond G3 is 56 m away and lies in terrain identical to that of G2, but it is shallower, with a depth usually of only 0.3 m. Pond G3 is a characteristic hard-bottomed pond. Diaptomus shoshone was found here in 30 of 32 sampled years, at densities ranging from 0.02-2.40/L; Chaoborus americanus appeared only twice (1979 and 1986; Table 1) and at low densities ([less than or equal to]0.03/L). Only two midge larvae were found during their most recent appearance (1986), which was a heavy snowpack year (82.8 cm).

Ponds G5 and G6, the second pair of ponds, are situated 38 m apart and 1.7 km distant from G2 and G3; G6 is a little deeper and has a softer bottom. The hard-bottomed G5 maintained a Diaptomus shoshone-dominated community throughout the sampling period, with a few Chaoborus americanus present only in 1979 and 1981, which is when D. shoshone had low abundance (too shallow to be measured quantitatively). Since 1988 in pond G5, D. shoshone densities have been high, to over 4.2/L, and C. americanus have been absent.

The slightly greater depth and softer bottom of pond G6 have facilitated the more regular occurrence of Chaoborus americanus in this water body. For 14 y, including the low snowpack years of 1987 and 2001, only Diaptomus shoshone was present; for 8 y, including the heavy snowpack years of 1996 and 1997, only C. americanus was present; and for 7 y, both invertebrate predators occurred together. For those years when C. americanus was the only predator, the snowpack on 15 May the previous year averaged 67.0 [+ or -] 19.1 cm (n = 8), and for those years when only D. shoshone was found, the snowpack on 15 May the previous year averaged 55.1 [+ or -] 24.1 cm (n = 14; mean [+ or -] SD). The difference in snowpack over these sets of years did not differ statistically ([t.sub.17] = 0.590, n.s.). As with pond G2, extreme snowpack values correlated with shifts in predator dominance: one year following the extremely low snowpacks of 1987 and 2001, the community shifted to D. shoshone, and following the extremely high snowpack years of 1996 and 1997, the community returned to C. americanus dominance. The difference in snowpack just missed significance when the data for ponds G2 and G6 were analyzed in aggregate ([F.sub.1,42] = 2.298, one-tailed P = 0.069).

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

However, because these two invertebrate predators can eat each other, their densities displayed a reciprocal response. Chaoborus americanus densities were lower (0.02 [+ or -] 0.02/L) when both species were present than when the midge larvae were alone (0.13 [+ or -] 0.12/L); similarly, Diaptomus shoshone densities were lower (0.14 [+ or -] 0.16/L) when C. americanus was present than when it was absent (0.70 [+ or -] 0.83/L). Based on all observations when the species were found together from 1974 to 2009 (5 y in each of G2 and G6 ponds and once in G3), a reciprocal response in the logs of their densities was apparent (Fig. 2), with a significant negative correlation ([F.sub.1,9] = 57.17, P < 0.001).

DISCUSSION

An early study of high elevation ponds in this mountainous region found that, while bodies of water with inlets and outlets supported fish populations with distinct plankton communities, the pond communities represented two distinct types: those dominated by Chaoborus americanus and those characterized by the presence of Diaptomus shoshone (Williams, 1976). Because chaoborids must overwinter as larvae, they survive in ponds that retain water year round and have a layer of organic mud at the bottom. Williams (1976) showed that the mud provides a nonfreezing refuge during winter for chaoborid larvae. These ponds are typically surrounded by a dense growth of sedges. In contrast, any pond that either dries fully by the end of summer or freezes completely to the bottom over winter cannot support overwintering Chaoborus larvae. Instead, D. shoshone, which overwinters as encysted eggs, are typically found in the plankton communities of these harder bottomed ponds. Encysted eggs can sometimes be found in the pond bottoms when dry (pers. obs.).

The effect of snowpack on predator dominance was most noticeable in pond G2. In average snowpack years, this pond retained enough water to avoid freezing completely or drying up, and in these years Chaoborus americanus was the dominant predator and Diaptomus shoshone was absent. Following the very low snowpack yeas of 1987, however, D. shoshone appeared. It reappeared again after another dry year (2001), when C. americanus density dropped dramatically. As expected, pond G3, close to G2 and shallower with a harder bottom, retained a D. shoshone predatory regime throughout the 36 y period. Similar results were found for the other pair of ponds, with the hard-bottomed G5 retaining dominance by D. shoshone while the softer-bottomed G6 changed in predatory regime. As with G2, the changes in G6 were associated with extreme snowpack levels. This study gives some evidence that, as hypothesized, weather influenced major shifts in the predatory regime of the invertebrate predators. The strongest result is that the effect was most obvious with extreme snowpack levels. Other effects of weather on pond communities have been documented by George (2000), who found an increase in algal growth with higher temperatures and thus increased zooplankton abundance, and by Drenner et al. (2009), who reported that drying in pond communities altered fish predation.

The occasional appearance of Chaoborus americanus in the four study ponds shows that flying adults can readily disperse their eggs to different bodies of water. Fourth instars exert stronger feeding pressure on the rest of the pond community than do earlier instars (Williams, 1980; Swift, 1992), so those midge larvae that survive the winter in a pond and then reach the large size of later instars become the most important predators during the following summer. After C. americanus has been eliminated from a pond through drying or complete freezing, Diaptomus shoshone may become reestablished through wind or water mediated dispersal of eggs or through hatching of diapausing eggs from what is the egg equivalent of a seed bank (Parker et al., 1996). Feeding by D. shoshone adults on first instar chaoborids prevents the predatory regime from switching back. The feeding of these two invertebrate predators, C. americanus and D. shoshone, on each other leads to reciprocity of their densities when they occur together and to their frequently disjunct distribution, as shown here and reported initially in Williams (1980).

Weather is not the only factor that influences these pond communities. The study area is in a national forest (Shoshone N.F.), and late in the summer of some years, grazing sheep brought up to high elevations may contribute to nutrient loading of the drainage area of a pond. Increased nutrients may promote the growth of sedges, which add decaying organic matter and increase the softness of the pond bottom. This change, in turn, could facilitate overwinter survival of Chaoborus larvae and potentially alter the predatory regime of a pond community, but no examples were apparent in this study.

Few studies examine predatory effects for a time frame longer than several years (examples are Bell et al., 2003; Findlay et al., 2005), so the evidence presented here about dynamism in predatory regimes of high elevation ponds provides an unusual long term perspective of the effect of weather and the pattern of community responses. These results demonstrate the importance of extreme events, too; average snow depth did not lead to changes in the predators, but the years with the most and least snow did correlate with switching of predatory regimes. Climate change may lead to a long term decline in winter snowpack, so pond communities could shift towards predators and coexisting species that are more tolerant of drying.

Acknowledgments.--I thank Hamilton College for supporting my fieldwork over many years; Bill Pfitsch, two reviewers, and an editor for comments on the manuscript; and Sharon Williams and Anne Williams (posthumously) for their support and assistance in the field.

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SUBMITTED 10 FEBRUARY 2011

ACCEPTED 31 OCTOBER 2011

ERNEST H. WILLIAMS (1)

Department of Biology, Hamilton College, Clinton, New York 13323

(1) e-mail: ewilliam@hamilton.edu
TABLE 1.--Summary of long term sampling of four ponds in the
Beartooth Mountains, northwest  Wyoming, from 1974 through 2009.
Physical characteristics and the presence of Diaptomus shoshone
(Ds) and Chaoborus americanus (Ca) are shown

                             Max
         Elev    Surface    depth
Pond     (m)    area (ha)    (m)    Latitude

G2       3021     0.24       0.5    44[degrees] 55'34"E
G3       3022     0.13       0.3    44[degrees] 55'35"E
G5       2908     0.33       0.4    44[degrees] 56'05"E
G6       2906     0.07       0.4    44[degrees] 56'05"E

                                            Years with
                                 Years
Pond     Longitude              sampled   Ca    Ds    Both

G2       109[degrees] 33'00"N     31      19    7      5
G3       109[degrees] 33'04"N     32      2     29     1
G5       109[degrees] 31'50"N     30      0     28     2
G6       109[degrees] 31'47"N     29      8     14     7
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