© 2002 by The Society for Integrative and Comparative Biology
| ||||||||||||||||||||||||||||||||||||||||||||||||||||
Biogeography, Competition, and Microclimate: The Barnacle Chthamalus fragilis in New England1
1 Department of Biological Sciences, University of South Carolina, Columbia, South Carolina 29208
 |
SYNOPSIS |
|---|
TOP
 SYNOPSIS INTRODUCTIONTESTS OF HYPOTHESESDISCUSSIONReferences |
|---|
Geographic limits of species are commonly associated with climatic or physical boundaries, but the mechanisms of exclusion at the limits of distribution are poorly understood. In some intertidal populations, the strengths of interactions with natural enemies are mediated by microclimate, and determine geographic limits. The northern limit of the barnacle Chthamalus fragilis in New England is the south side of Cape Cod, Massachusetts. South of the cape, Chthamalus has a refuge from competition in the high intertidal, which is too hot for survival of its superior competitor Semibalanus balanoides. North of the cape, the high intertidal is cooler, and Semibalanus survives, so Chthamalus has no refuge. Thus, geographic variation in the strength of competition may determine the geographic limit of Chthamalus. Intolerance of cold by Chthamalus cannot account for the geographic limit: transplants of Chthamalus 80 km beyond its northern limit survived up to 8 yr in the absence of competition with Semibalanus. At the geographic limit of Chthamalus in the Cape Cod Canal there are two bridges, 5 km apart. On the southern bridge, Chthamalus is abundant and occupies a refuge above Semibalanus. On the northern bridge in 2001, only 7 individual Chthamalus were present. Despite the proximity of the bridges, their microclimates are very different. The southern bridge, where Chthamalus is abundant, is up to 8°C hotter than the northern bridge. This higher temperature creates a refuge in the high intertidal for Chthamalus. On the cooler northern bridge, there is no refuge for Chthamalus. Because of the difference in temperatures of the water masses that meet in the canal, heat storage in the rock of the bridge piers causes the temperatures to differ between the bridges. Thus, geographic change in microclimate alters the strength of competition, and determines the geographic limit.
"When we travel from south to north, or from a damp region to a dry, we invariably see some species gradually getting rarer and rarer, and finally disappearing; and the change in climate being conspicuous, we are tempted to attribute the whole effect to its direct action. But this is a very false view: we forget that each species, even where it most abounds, is constantly suffering enormous destruction at some period of its life, from enemies or from competitors for the same place and food; and if these enemies or competitors be in the least degree favoured by any slight change of climate, they will increase in numbers, and as each area is already fully stocked with inhabitants, the other species will decrease."—Charles Darwin, On the Origin of Species, 1859, p. 69.
|
INTRODUCTION |
|---|
|
TOP
SYNOPSISINTRODUCTIONTESTS OF HYPOTHESESDISCUSSIONReferences |
|---|
In this paper I pose the question "what mechanisms set the geographic limits of species?" When considering the northern and southern limits of species, we tend to put our minds into an autecology framework, in which we think of species in isolation and assume that they are limited by intolerance of cold at their pole ward limits and by intolerance of heat at their equator ward limits. This approach was formalized very elegantly by Hutchins (1947)
. He made the case that geographic limits are set by thermal tolerances of the most sensitive life stages. He showed that one could take advantage of the differences in temperature on opposite sides of the Atlantic and Pacific to determine which kind of limitation was occurring at the northern and southern extent of species ranges. This approach, although appealing, is in opposition to the rest of the way ecologists view systems, where interactions among species are commonly the foci of our studies.
I will take a community ecologist's view of biogeography and turn several of these ideas upside down. In the end, I will demonstrate that the northern limit of a tropical species is set not by intolerance of cold, but rather in a strange way, by intolerance of heat. I also hope to demonstrate that interaction strength in the community is the key factor that explains the geographic pattern (e.g., Darwin, 1859, p. 69). I will use a combination of field experiments, purely descriptive ecology, biophysical ecology and models to dissect out the underlying mechanisms.
On the basis of field manipulations of microclimate, I have argued that the same mechanisms responsible for creating local vertical zonation patterns, also determine the northern geographic limit of the barnacle Chthamalus fragilis in New England (Wethey, 1983, 1984). Chthamalus has a geographic range from the Caribbean to the south side of Cape Cod (Dando and Southward, 1980). Near its northern limit, Chthamalus lives in a narrow band in the high intertidal zone, below which lives the boreo-arctic barnacle Semibalanus balanoides. This zonation is the result of competition between the species. When I removed the competitively dominant Semibalanus from the low intertidal, Chthamalus invaded and persisted (Wethey, 1983). Connell (1961) had similar results near the northern limit of Chthamalus in Scotland.
Local microclimate strongly determines the local zonation of the two species. On north-facing vertical surfaces, Chthamalus occupies a narrow zone; on south-facing verticals it occupies a wider zone, and on nearly horizontal surfaces, its zone is even broader (Wethey, 1983). Figure 1 illustrates this pattern very clearly. The area between the black lines is the Chthamalus zone, and the region below the lower black line is the Semibalanus zone. On sloping surfaces of the left hand boulder, Chthamalus occupies a wider zone than on the vertical surfaces (Fig. 1). The mechanism responsible for this pattern involves the mediation of interaction strength by microclimate. The low shore competitive dominant Semibalanus is intolerant of heat and desiccation, and its upper shore limit of distribution is strongly influenced by direct solar radiation (which contributes the largest component of heating in the system). Chthamalus is extremely resistant to heat and desiccation (Southward, 1958; Foster, 1969, 1971a, b), able to withstand rock temperatures up to 45°C (Aveni-Deforge and Wethey, 2001). In microhabitats where Semibalanus survives, it competitively excludes Chthamalus. I demonstrated this experimentally by placing opaque shades over small areas of shore, using clear plastic roofs as controls. In shade treatments, Semibalanus recruits survived on the upper shore and were responsible for 94% of the mortality of Chthamalus by crushing, undercutting and overgrowing. In the sun treatments, more than 90% of the Semibalanus recruits died, and Chthamalus suffered little mortality (Wethey, 1984).
|
North of Cape Cod, Semibalanus is only slightly affected by local microclimate (Wethey, 1983
, 1984). Semibalanus survives over the entire intertidal zone in northern New England, even when it dies back further south. In consequence, I hypothesized that north of Cape Cod, Chthamalus has no refuge from competition on the high shore, and it is therefore excluded from northern New England (Wethey, 1983, 1984; see also Southward and Crisp, 1956; Lewis, 1964, p. 252).
Distribution of Chthamalus near its northern limit
The geographic distribution of Chthamalus around its northern limit (Fig. 2) has a very sharp boundary at Cape Cod, Massachusetts. On the south side of Cape Cod, from Woods Hole to the western half of the Cape Cod Canal (completed in 1914), Chthamalus forms a dense band in the high intertidal. In these areas, Chthamalus can occupy up to 100% of the available substratum in the refuge zone. Two highway bridges, built in the 1930s cross the canal, approximately 5 km apart. The Bourne Bridge (41°44'50''N, 70°35'25''W) is nearer the western end of the canal and its barnacle populations are more representative of southern New England distributions, with a dense (10 per 0.01 m2) Chthamalus band in the high intertidal zone (Fig. 2). The Sagamore Bridge (41°46'33''N, 70°32'37''W), is near the eastern end of the canal and its barnacle populations are more characteristic of northern New England, with very few Chthamalus. In 1983, there were between 0.1 and 0.5 Chthamalus per 0.01 m2 at the top of the barnacle zone on the Sagamore Bridge. In 2000–2001, only 7 Chthamalus individuals were alive on the north piers of the bridge, representing a population density of 0.09 per 0.01 m2 at the top of the barnacle zone. The sharp change in population density between the two bridges on the Cape Cod Canal is remarkable because it takes place over a distance of 5 km.
|
In this paper I examine two hypotheses that might explain the geographic distribution of Chthamalus near its northern limit. The strict microclimate hypothesis is that Chthamalus is limited to the region south of Cape Cod by intolerance of cold. I tested this experimentally with a transplant. The combined microclimate-competition hypothesis is that the refuge from competition disappears as one crosses the geographic limit. To test this hypothesis, first I quantified the microclimatic conditions associated with the refuge zone. I hypothesized that the difference in water temperature between the colder Massachusetts Bay to the north and the warmer Buzzards Bay to the south caused the intertidal shore temperatures to differ at low tide. Shore temperatures could differ if there was heat storage in the rock, and if the rate of heat conduction to and from the rock was high enough to affect the surface temperature of the rock. I tested this hypothesis by quantifying the temperatures experienced by Chthamalus on the two bridges, and by developing a numerical model of rock temperature with which I could examine the effect of the heat storage terms on the temperature of the rock.
|
TESTS OF HYPOTHESES |
|---|
|
TOP
SYNOPSISINTRODUCTIONTESTS OF HYPOTHESESDISCUSSIONReferences |
|---|
A test of the intolerance of cold hypothesis
To test the hypothesis that the northern limit of Chthamalus is set by intolerance of cold conditions to the north, I transplanted Chthamalus beyond their northern limit, and measured their survival. Stones and plastic disks with Chthamalus from the Yale Field Station in Connecticut (41°16'N, 72°44'W), 180 km south of the northern limit, were transported by car at night to avoid overheating, and glued with epoxy to the intertidal zone in Nahant Massachusetts (42°25'02''N, 70°54'25''W), 80 km beyond the northern limit. Water temperatures are lower in Massachusetts than in Connecticut (12°C lower in August 1990, 4°C lower in June 2001).
Transplants were divided into several treatments:
- Vertical surface in Semibalanus zone, exposed to competition.
- Vertical surface in Semibalanus zone, competitors removed in spring 1984.
- Horizontal surface in Semibalanus zone, exposed to competition.
- Horizontal surface in Semibalanus zone, competitors removed in spring 1984.
- Vertical surface above Semibalanus zone, where there is no natural barnacle settlement, and therefore no competition.
- Vertical surface in Semibalanus zone, competitors removed in spring 1984.
Chthamalus that were transplanted to the Semibalanus zone at Nahant died rapidly if exposed to competition from Semibalanus, but survived well in treatments where competitors had been removed (Fig. 3a). This result was similar both on vertical and horizontal surfaces (Fig. 3a, b). Most remarkably, Chthamalus survived as long as 8 yr in the zone above the upper limit of settlement and survival of Semibalanus (Fig. 3c). Since the upper limit of settlement of larvae is approximately the same in both Chthamalus and Semibalanus (Wethey, 1983), the zone of treatment (e) is an area where recruitment cannot or does not occur. However, if transplanted to this zone, Chthamalus can survive for very long periods, far longer than Semibalanus. The maximum lifespan of Semibalanus in the high intertidal at Nahant, Massachusetts is approximately 3 yr (Wethey, 1985), compared to the 8 yr lifespan of the Chthamalus transplants (Fig. 3c). Therefore Chthamalus survives very well in areas beyond its northern limit, but only at shore levels where it cannot settle and recruit naturally, or where its competitor is experimentally removed. These results are consistent with the hypothesis (Southward and Crisp, 1956; Lewis, 1964; Wethey, 1983, 1984) that Chthamalus is not limited by cold at its northern limit, but rather by competition with Semibalanus.
|
Tests of the combined microclimate—competition hypothesis
Quantification of the conditions in the Chthamalus refuge zone
To quantify the refuge of Chthamalus from competition, I measured the upper zonation limits of both Chthamalus and Semibalanus on rock surfaces with a variety of slopes and orientations to the sun in June and July of 1983 and 1984 at sites in Long Island Sound on Horse Island (41°15'N, 72°45'W), and the Yale Peabody Museum Field Station (41°16'N, 72°44'W), Connecticut. Elevations of all sites were measured with a telescopic contractor's level and leveling rod, and referenced to a benchmark of known elevation at the Yale Field Station. Slopes and orientations of the rock surfaces at the zonation limits were measured with an inclinometer and sighting compass (Silva Ranger). Magnetic orientations were corrected for local magnetic declination using published values on U.S. Geological Survey topographic maps of the region, for the period 1983–1984. A total of 140 elevations were measured.
If body temperature affects Semibalanus survival as suggested by Figs. 1 and 3, then the upper shore zonation limit should correlate more strongly with temperature for Semibalanus than for Chthamalus. The thermal conditions at each of the zonation limits were estimated using a numerical model of rock temperature. The model was derived from methods described in Denny and Wethey (2001) (see Fig. 7 for model validation). Since barnacles are so small, and since they have a large surface area in contact with the rock, their temperatures were assumed to be the same as the rock (Thomas, 1987; Bertness, 1989). The model uses air temperature, water temperature, height of the tide, and solar radiation at 10-min intervals, to predict the surface temperature of the rock. Solar radiation was calculated from the position of the sun in the sky, assuming a maximum solar irradiance of 1,000 W m–2. The position of the sun in the sky was calculated at 10-min intervals for June 1983 and June 1984 using the NASA-JPL long ephemeris (Giorgini et al., 1996). Air temperatures for East Wareham Massachusetts, in June 1983 and June 1984 were used as proxies for air temperatures in Connecticut. East Wareham is 180 km east of the study sites in Long Island Sound, and has very similar climate. Water temperatures at New London Connecticut for June 1997 were used as a proxy for water temperature in Long Island Sound in June 1983 and 1984. The air temperature conditions in 1983–84 and 1997 were similar. New London is 55 km east of the sites where barnacle zonation was quantified. Tidal elevations were calculated at 10-min intervals for June 1983 and 1984 with the computer program WXTide (Flater, 2000), which uses the U.S. National Oceanic and Atmospheric Administration (NOAA) tidal prediction algorithms (Schureman, 1958). The maximum predicted rock temperature at each of the barnacle survey locations was used as a summary of the thermal conditions at that site.
|
As expected, the rock temperature model results indicate that the upper zonation limit of Semibalanus moves down the shore as maximum rock temperature increases (Fig. 4). In the figure, the lines represent the linear regression of the height of the empirically measured zonation limit versus the predicted maximum rock temperature, and the 95 percent confidence band around the individual estimates. The solid lines are for Semibalanus, dotted lines are for Chthamalus. The upper zonation limit of Chthamalus is less sensitive to maximum rock temperature as seen by the smaller slope of its regression line (Fig. 4). The refuge for Chthamalus from competition is the triangular region in the upper right hand corner of the graph, where Chthamalus survives above the upper zonation limit of Semibalanus. The refuge is the region where Chthamalus lives above the 95% confidence band of Semibalanus distribution limit. The refuge does not exist when the maximum rock temperature is below 26°C (Fig. 4). The refuge increases in size as the maximum rock temperature increases. As maximum rock temperatures increase above 26°C, the refuge expands from a small region at +2.2 m above MLW to a zone spanning +1.5 m to +1.8 m above MLW when the maximum temperature are 40°C. Semibalanus was not found in sites whose maximum predicted temperatures exceeded 42°C (Fig. 4).
|
Hypotheses that might explain the sharp boundary within the Cape Cod Canal
The distribution of Chthamalus (Fig. 2) corresponds to a large water temperature difference between the two ends of the Cape Cod Canal, with cold water on the Massachusetts Bay (north) side and warmer water on the Buzzards Bay (south) side. The temperature difference is as much as 12°C. The tidal range is 1.22 m in Buzzards Bay and 2.86 m in Massachusetts Bay, where the mean tide level is 0.12 m lower. High tide in Massachusetts Bay is approximately 3 hr later than Buzzards Bay. As a result, there is a current that reverses every 6 hr and reaches a mean maximum velocity of 2 m sec–1. Although the water temperature in the canal shifts throughout the tidal cycle, at high tide the Bourne Bridge is immersed in warmer Buzzards Bay water (Fig. 5) and the Sagamore Bridge is immersed in colder Massachusetts Bay water. As a result of convective heat exchange during immersion, and heat storage in their granite blocks, the piers of the Bourne Bridge are likely to begin each low tide at a higher temperature than those of the Sagamore Bridge. Heat conduction within the piers is then likely to be an important contributor to temperature excursions of the surfaces of the piers at low tide. These factors are likely to cause the temperatures of barnacles on the piers to be higher on the Bourne Bridge than on the Sagamore Bridge, at equivalent tidal heights. These temperature differences may be responsible for the presence of a Chthamalus refuge zone on the Bourne Bridge and the absence of one on the Sagamore Bridge (Fig. 2).
|
To test the hypothesis that the southern bridge is consistently warmer than the northern bridge at low tide, temperature recordings were made at the upper distribution limits of Chthamalus and Semibalanus on both bridges. Small self contained temperature data loggers (Thermochron model 1921 iButton, Dallas-Maxim Semiconductor Corporation) were glued to the piers of the Bourne and Sagamore Bridges with underwater epoxy putty (Splash-Zone Compound, Z Spar Corporation). The loggers are similar in shape to a watch battery (stainless steel case, 17 mm diameter, 5 mm thick), and were programmed to record observations every 30 min for 45 days, at a resolution of 0.5°C. The loggers were programmed and data were downloaded with a Palm-Pilot hand held computer interface (IConnection model 3301A, Scanning Devices Corporation).
The southern bridge is consistently warmer than the northern bridge. On north-facing surfaces of the northern (Sagamore) bridge, the temperature exceeded 26°C on only 1 low tide in 2001, yet on surfaces of similar aspect on the southern (Bourne) bridge, the temperature commonly exceeded 26°C during low tides throughout the summer of 2001 (Fig. 6). On south facing surfaces of the two bridges the temperatures are higher and there is a consistent difference between the northern and southern bridges. On the south facing surfaces of the Sagamore bridge the temperature exceeded 32°C on only 1 low tide in 2001, whereas on south facing surfaces at the same tidal height on the Bourne bridge, the temperature exceeded 32°C on 15 low tides (Fig. 6). Chthamalus should have a refuge from competition only on surfaces whose maximum temperature exceeds 26°C (Fig. 4). The refuge from competition becomes large when the maximum surface temperature exceeds 32°C (Fig. 4). These results indicate that the southern Bourne Bridge has thermal conditions consistent with the presence of a refuge from competition for Chthamalus, and the northern Sagamore Bridge does not.
|
In order to determine whether heat storage in the piers of the bridges could account for the difference in low tide conditions on the two bridges, the numerical model of rock temperature (see above) was used to simulate rock temperatures during the period June 1 to June 20, 2001. Water levels at the two bridges were obtained from 6-min records for June 2001 from tide gauges deployed by NOAA, adjacent to each bridge. The Bourne tide gauge (Canal Station 320) was 304 m west of the bridge, and the Sagamore tide gauge (Canal Station 115) was 730 m east of the bridge. Water temperatures for Massachusetts Bay were from the NOAA tide station in Boston, and water temperatures for Buzzards Bay were from the NOAA tide station in Woods Hole, for the same period. Air temperatures for the period were from the NOAA cooperative weather station at East Wareham (41°46'N, 70°40'W), 6.5 km west of the Bourne Bridge. Solar radiation was estimated using calculated azimuths and elevations of the sun for the same dates and times of day, calculated with the NASA-JPL long ephemeris (Giorgini et al., 1996
). Two model scenarios were used. One scenario used the normal pattern of colder water on the Massachusetts Bay end of the canal and warmer water on the Buzzards Bay end of the canal. In order to test the hypothesis that differences in water temperature during immersion could change the rock temperatures during low tide, in the second model scenario the northern bridge was exposed to simulated southern water temperatures and the southern bridge was exposed to simulated northern water temperatures, while maintaining the normal tidal oscillations at each site. The model predicts very well the timing and magnitude of temperature fluctuations during low tide (Fig. 7). Since the model was based on idealized solar radiation values, much of the difference between the model and the observed temperatures are likely the result of clouds and rainy conditions that occurred on some of the days during the model run (July 2 and 4).
If heat storage in the piers of the bridge were important, then differences in water temperature at high tide should be reflected in temperature differences at low tide. The results of the simulation indicate that heat storage in the piers of the bridges accounts for at least 2°C of the temperature difference between the bridges. The mean difference in water temperature between the north and south sides of the canal during the period of the model runs was 4.4°C. In the simulations where northern bridge was exposed to southern water at high tide, the rock temperatures at low tide were on average 2°C hotter (maximum of 5.4°C hotter) in the simulations where it was exposed to northern water at high tide. In the simulations where the southern bridge was exposed to southern water at high tide, rock temperatures were on average 2°C hotter (maximum of 6.1°C hotter) than in the simulations where it was exposed to northern water at high tide. If the northern bridge were exposed at high tide to warmer water from the south, it would create a small refuge for Chthamalus in the highest sites on the piers.
|
DISCUSSION |
|---|
|
TOP
SYNOPSISINTRODUCTIONTESTS OF HYPOTHESESDISCUSSIONReferences |
|---|
This paper examines the mechanisms responsible for setting the geographic limits of species. It specifically tests two general classes of hypotheses regarding polar limits: 1) that species are strictly limited by intolerance of physical conditions beyond their polar limit (the intolerance of cold hypothesis), and 2) that species are limited by interactions with natural enemies, whose strength is a function of physical conditions (the combined microclimate-competition hypothesis).
The intolerance of cold hypothesis was falsified by the results of the transplant experiment. Chthamalus survived up to 8 yr in transplants 80 km beyond its northern limit, in areas where its competitor could not settle and survive (Fig. 3). At the same geographic location Semibalanus survives typically no more than 3 yr in the high intertidal zone (Wethey, 1985). The evidence in Britain is similar. In Europe, the northern and eastern limit of Chthamalus is near Aberdeen on the east coast of Scotland, the Isle of Wight and the Cap de la Hague west of Cherbourg on the English Channel (Crisp et al., 1981). Crisp (1950) transplanted Chthamalus stellatus beyond its northern limit to the North Sea coast at Whitley Bay, Northumberland, where it survived two winters and produced viable larvae. In the extraordinarily cold winter of 1962–63, Chthamalus did not suffer increased mortality, although other subtropical species did (Crisp, 1964). At its northern geographic limit both in New England and in Britain, Chthamalus is most abundant at the highest shore levels, where the effect of cold would be the greatest. If Chthamalus were intolerant of cold, it should die in winter at its northern limit, however this does not appear to be the case (Crisp and Southward, 1958; Lewis, 1964, pp. 251–252; Wethey, 1984). Additionally, since larval stages tend to be more sensitive to environmental conditions than adults (Southward, 1958; Crisp and Ritz, 1967; Foster, 1969, 1971a, b), the fact that Chthamalus settles in autumn near its northern limit (Hatton, 1938; Wethey, 1983, 1984; Lewis, 1986; O'Riordan et al., 1995) suggests that all life stages of Chthamalus are tolerant of cold.
The results of this study are consistent with the hypothesis that the strength of interactions with natural enemies determines the geographic limit. Chthamalus fragilis in southern New England has a refuge from competition whose size is correlated with the maximum temperature reached by the rock surface in summer (Fig. 4). In sites with a maximum temperature below 26°C, there is no real refuge. The size of the refuge increases with temperature above 26°C (Fig. 4). When maximum rock temperature is above 40°C, the refuge can be 20 cm or wider (Fig. 4). Above 42°C, Semibalanus appears to be unable to survive (Fig. 4). This is consistent with the observation that Semibalanus balanoides enters heat coma between 35°C and 37°C, and that its LT50 is 44.3°C (Southward, 1958; Foster, 1969). Presumably the competitive ability of Semibalanus is greatly impaired when it is in heat coma. Selective death of some Semibalanus genotypes in high temperature microhabitats (Schmidt and Rand, 1999, 2001) may also affect average competitive ability. Chthamalus stellatus reaches heat coma at 43°C and its LT50 is approximately 50°C (Southward, 1958; Foster, 1969). Chthamalus fragilis presumably has similar tolerance for heat to C. stellatus so it is likely to take advantage of the competition refuge where conditions are too hot for Semibalanus. In South Carolina, Chthamalus fragilis survives on rock surfaces that commonly reach temperatures above 40°C, and withstands rock temperatures of 45°C (Aveni-Deforge and Wethey, 2001).
The geographic limit of Chthamalus appears to be in the middle of the Cape Cod Canal, which connects the warm waters of Buzzards Bay, south of Cape Cod, to the cold waters of Massachusetts Bay, north of Cape Cod (Fig. 2). There is a refuge from competition for Chthamalus on the southern of two highway bridges across the Cape Cod Canal, because the piers of the bridge store heat from the warm water of Buzzards Bay, and warm up to high enough temperatures that Semibalanus dies in the high intertidal zone. There is no refuge for Chthamalus on the northern of the two highway bridges; the piers remain colder at low tide because they are immersed at high tide in the colder water of Massachusetts Bay. The importance of heat storage in the substratum documented here is consistent with Bertness' (1989) observations that large intertidal boulders and cobbles embedded in the substratum remain cooler than loose cobbles. This sort of fine balance between the two species near their geographic limits is consistent with the 40 yr of observations by Southward (1991), who found that Semibalanus increased at the expense of Chthamalus after summers with cooler sea surface temperatures in southern England.
The temperature differences observed here between the bridges on the Cape Cod Canal have similar biological effects over a much larger geographic scale on opposite sides of the cape. Leonard (2000) compared Semibalanus balanoides zonation, recruitment, survival, and growth between sites north of Cape Cod (Damariscotta, Maine) and south of Cape Cod (Newport, Rhode Island). He found that Semibalanus survived higher on the shore in Maine than in Rhode Island, consistent with my observations in Massachusetts and Connecticut (Wethey, 1983, 1984, this paper). His temperature measurements indicate that the Rhode Island sites were hotter than those in Maine (Leonard, 2000). In addition, he found that shade from algal canopies enhanced Semibalanus survival in Rhode Island, but not in Maine. Bertness (1989), working in Rhode Island, found that crowded Semibalanus on cobbles had lower body temperatures and higher survival than solitary individuals on cobbles of similar size. These results are consistent with the observation that Semibalanus dies back from hot exposed sites on the high shore south of Cape Cod (Fig. 3). Based on the results of the present paper, the positive effect of density in Semibalanus should disappear north of Cape Cod, where thermal stress is reduced. This expectation is consistent with my (Wethey, 1979, p. 69) observation north of Cape Cod, that crowded Semibalanus in the high intertidal had lower survival than solitary individuals, a pattern opposite to that observed south of Cape Cod by Bertness (1989).
The results of the heat model indicate that the thermal conditions during high tide have a potentially important influence on temperatures experienced by barnacles at low tide, because of heat storage in the rock, and the conduction term in the heat equation. As we have moved to more mechanistic models of intertidal thermal conditions, we have tended to assume that sub aerial conditions were rather independent of submerged conditions. However for organisms whose temperatures are largely influenced by their substratum, like limpets (Hayworth and Quinn, 1990) and barnacles (Thomas, 1987; Bertness, 1989), sea surface temperature has an influence on body temperatures at low tide via heat storage in the rock. This is in contrast to organisms that sit above the substratum, like mussels, whose body temperature at low tide is more weakly influenced by sea surface temperature (Helmuth and Hoffman, 2001).
Failure of recruitment could also determine the location of a geographic limit. Lewis et al. (1982) hypothesized that recruitment failure may set the northern limit of Chthamalus in Scotland. However, in New England, especially in the Cape Cod Canal, this is very unlikely. There is a very fast current that moves back and forth with the tides in the canal, and there are dense populations (10 per 0.01 m2) of Chthamalus on the western half of the canal. It is hard to imagine how Chthamalus larvae could fail to be transported to the eastern half of the canal in this hydrodynamic environment.
The community ecology approach to thermal tolerances of organisms is very useful in developing predictive models of biogeographic distribution. Since the strengths of interactions in communities help determine the distribution and abundance of species, it should not be terribly surprising that such interactions may influence the geographic distribution of species (e.g., Darwin, 1859). In the case of Chthamalus fragilis in New England, it is the interplay between the thermal environment and the strength of competition with Semibalanus balanoides, which varies geographically and determines the geographic limit of distribution (confirming the conjectures by Southward and Crisp [1956], Lewis [1964], and Wethey [1983]).
|
ACKNOWLEDGMENTS |
|---|
This work was supported by the National Science Foundation (field work: OCE 82-08176, OCE 86-00531; data analysis: DEB-0108412). Sarah Woodin helped in all phases of this project, and improved the manuscript. Richard Grosberg, Matthew Reed, and Ron Etter, assisted in the field work during the 1980s. Leo Buss provided access to the Yale Peabody Museum Field Station and to Horse Island, and provided housing and transportation in the 1980s. Frank Ciccone, Engineer in Charge, US Army Corps of Engineers Cape Cod Canal Field Office permitted access to the Cape Cod Canal bridges, and Frank Morris, Assistant Engineer in Charge, provided engineering drawings of the elevations of the bridge piers, and water temperature data. Nathan Riser, Robert Shepard, Henry Werntz, Kenneth Sebens, and Joseph Ayers, directors of the Northeastern University Marine Science Center at Nahant, provided access to study areas. M. Patricia Morse provided housing and transportation in Massachusetts in the 1980s. Brian Helmuth introduced me to Ibuttons. Dave Chanoux of Scanning Devices Inc. provided software support for the Ibutton/Palm Pilot interface. This paper is dedicated to Jack Lewis who started my interest in geographic limits of species, and for whom this is merely confirmation of what he knew in 1964.
|
FOOTNOTES |
|---|
1 From the Symposium Physiological Ecology of Rocky Intertidal Organisms: From Molecules to Ecosystems presented at the Annual Meeting of the Society for Comparative and Integrative Biology, 2–7 January 2002, at Anaheim, California.
2 E-mail: wethey{at}biol.sc.edu
|
References |
|---|
|
TOP
SYNOPSISINTRODUCTIONTESTS OF HYPOTHESESDISCUSSIONReferences |
|---|
Aveni-Deforge, K., and D. S. Wethey. 2001. Physical constraints on zonation patterns of the barnacle Chthamalus fragilis. Amer. Zool, 41:1383.
Bertness, M. D. 1989. Intraspecific competition and facilitation in a northern acorn barnacle population. Ecology, 70:257-268.[CrossRef]
Connell, J. H. 1961. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology, 41:710-723.
Crisp, D. J. 1950. Breeding and distribution of Chthamalus stellatus. Nature, 166:311-312.[Medline]
Crisp, D. J.(ed.) 1964. The effects of the severe winter of 1962–63 on marine life in Britain. J. Anim. Ecol, 33:165-210.
Crisp, D. J., and D. A. Ritz. 1967. Changes in the temperature tolerance of Balanus balanoides during its life cycle. Helgoländer Wiss. Meeresunters, 15:98-115.[CrossRef]
Crisp, D. J., and A. J. Southward. 1958. The distribution of intertidal organisms along the coasts of the English Channel. J. Mar. Biol. Ass. U. K, 37:157-208.
Crisp, D. J., A. J. Southward, and E. C. Southward. 1981. On the distribution of the intertidal barnacles Chthamalus stellatus, Chthamalus montagui and Euraphia depressa. J. Mar. Biol. Ass. U. K, 61:359-380.
Dando, P. R., and A. J. Southward. 1980. A new species of Chthamalus (Crustacea Cirripedia) characterized by enzyme electrophoresis and shell morphology: With a revision of the other species of Chthamalus from the western shores of the Atlantic Ocean. J. Mar. Biol. Ass. U. K, 60:787-831.
Darwin, C. 1859. On the origin of species by natural selection. John Murray, London.
Denny, M. W., and D. S. Wethey. 2001. Physical processes that generate pattern in marine communities. In M. D. Bertness, S. D. Gaines, and M. E. Hay (eds.), Marine community ecology, pp. 3–37. Sinauer Associates, Sunderland, Massachusetts.
Flater, D. 2001. WXTide. Flaterco. http://www.flaterco.com/xtide. (see also http://tbone.geol.sc.edu).
Foster, B. A. 1969. Tolerance of high temperature by some intertidal barnacles. Mar. Biol, 4:326-332.
Foster, B. A. 1971a.. Desiccation as a factor in the intertidal zonation of barnacles. Mar. Biol, 8:12-29.[Medline]
Foster, B. A. 1971b.. On the determinants of the upper limit of intertidal distribution of barnacles (Crustacea: Cirripedia). J. Anim. Ecol, 40:33-48.
Giorgini, J. D., D. K. Yeomans, A. B. Chamberlin, P. W. Chodas, R. A. Jacobson, M. S. Keensey, J. H. Lieske, S. J. Ostro, E. M. Standish, and R. N. Wimberly. 1996. JPL's on-line solar system data service. Bull. Am. Astr. Soc, 28:1158.
Hatton, H. 1938. Essais de bionomie explicative sur quelques espèces intercotidales d'algues et d'animaux. Annls. Inst. Océanogr. Monaco, 17:241-348.
Hayworth, A. M., and J. F. Quinn. 1990. Temperature of limpets in the rocky intertidal zone—effects of caging and substratum. Limnol. Oceanogr, 35:967-970.
Helmuth, B. S. T., and G. Hoffman. 2001. Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol. Bull, 201:374-384.
Hutchins, L. W. 1947. The bases for temperature zonation in geographical distribution. Ecol. Monogr, 17:325-335.[CrossRef]
Leonard, G. H. 2000. Latitudinal variation in species interactions: A test in the New England rocky intertidal zone. Ecology, 81:1015-1030.[CrossRef]
Lewis, J. R. 1964. The ecology of rocky shores. Hodder and Stoughton, London.
Lewis, J. R. 1986. Latitudinal trends in reproduction, recruitment and population characteristics of some rocky littoral molluscs and cirripedes. Hydrobiologia, 142:1-13.[CrossRef]
Lewis, J. R., R. S. Bowman, M. A. Kendall, and P. Williamson. 1982. Some geographical components in population dynamics: Possibilities and realities in some littoral species. Neth. J. Sea Res, 16:18-28.[CrossRef]
O'Riordan, R. M., A. A. Myers, and T. F. Cross. 1995. The reproductive cycles of Chthamalus stellatus (Poli) and C. montagui Southward in south-western Ireland. J. Exp. Mar. Biol. Ecol, 190:17-38.[CrossRef]
Schmidt, P. S., and D. M. Rand. 1999. Intertidal microhabitat and selection at MPI: Interlocus contrasts in the northern acorn barnacle, Semibalanus balanoides. Evolution, 53:135-146.[CrossRef]
Schmidt, P. S., and D. M. Rand. 2001. Adaptive maintenance of genetic polymorphism in an intertidal barnacle habitat: Habitat- and life-stage-specific survivorship of Mpi genotypes. Evolution, 55:1336-1344.[CrossRef][ISI][Medline]
Schureman, P. 1958. Manual of harmonic analysis and prediction of tides. Special Publication 98. U.S. Dept. of Commerce, Coast and Geodetic Survey, U.S. Government Printing Office, Washington, DC.
Southward, A. J. 1958. Note on the temperature tolerances of some intertidal animals in relation to environmental temperatures and geographic distribution. J. Mar. Biol. Ass. U. K, 37:49-66.
Southward, A. J. 1991. Forty years of changes in species composition and population density of barnacles on a rocky shore near Plymouth. J. Mar. Biol. Ass. U. K, 71:495-513.
Southward, A. J., and D. J. Crisp. 1956. Fluctuations in the distribution and abundance of barnacles. J. Mar. Biol. Ass. U. K, 35:211-229.
Thomas, F. I. M. 1987. The hot and cold of life on rocks: Determinants of body temperature in the northern rock barnacle, Semibalanus balanoides. Department of Ecology and Evolutionary Biology, Brown University, Providence, Rhode Island.
Wethey, D. S. 1979. Demographic variation in intertidal barnacles. Department of Biology, University of Michigan, Ann Arbor.
Wethey, D. S. 1983. Geographic limits and local zonation: The barnacles Semibalanus (Balanus) and Chthamalus in New England. Biol. Bull, 165:330-341.
Wethey, D. S. 1984. Sun and shade mediate competition in the barnacles Chthamalus and Semibalanus: A field experiment. Biol. Bull, 167:176-185.
Wethey, D. S. 1985. Catastrophe, extinction and species diversity: A rocky intertidal example. Ecology, 66:445-456.[CrossRef][ISI]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  J. Jost and B. Helmuth Morphological and Ecological Determinants of Body Temperature of Geukensia demissa, the Atlantic Ribbed Mussel, and Their Effects On Mussel Mortality Biol. Bull., October 1, 2007; 213(2): 141 - 151. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. W. Denny and C. D. G. Harley Hot limpets: predicting body temperature in a conductance-mediated thermal system J. Exp. Biol., July 1, 2006; 209(13): 2409 - 2419. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. W. Denny, L. P. Miller, and C. D. G. Harley Thermal stress on intertidal limpets: long-term hindcasts and lethal limits J. Exp. Biol., July 1, 2006; 209(13): 2420 - 2431. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. E. Gilman, D. S. Wethey, and B. Helmuth Variation in the sensitivity of organismal body temperature to climate change over local and geographic scales PNAS, June 20, 2006; 103(25): 9560 - 9565. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||