THE INFLUENCE OF INTERSPECIFIC COMPETITION AND OTHER FACTORS ON THE DISTRIBUTION OF THE BARNACLE CHTHAMALUS STELLATUS
Barnacle Distribution: Interspecific Competition and Other Factors
Interspecific competition in animals is primarily evidenced from laboratory populations.
Direct evidence of interspecific competition in nature is limited, leading to its sometimes minimized role in animal communities.
Indirect evidence suggests competition influences animal distribution in nature.
Species distribution range may decrease due to other species with similar needs.
Beauchamp and Ullyott 1932, Endean, Kenny and Stephenson 1956
Uniform space distribution often results from intraspecies competition.
Holme 1950, Clark and Evans 1954
Coexistence of similar animals indicates they avoid competition through niche differentiation.
Lack 1954, MacArthur 1958
Barnacle species (Chthamalus stellatus and Balanus balanoides) occupy separate zones with slight overlap on an intertidal rocky shore.
Chthamalus young are found in the lower zone but don't survive.
Hypothesis: Chthamalus is eliminated from the lower zone by Balanus due to competition for space.
Space for attachment and growth is limited in the rocky intertidal region.
Other factors influencing distribution were studied at Millport, Isle of Cumbrae, Scotland.
Thanks to Prof. C. M. Yonge and the Marine Station staff at Millport for assistance.
Gratitude to C. S. Elton, P. W. Frank, G. Hardin, N. G. Hairston, E. Orias, T. Park and students, and the author's wife for manuscript review.
Barnacle Species Distribution Details
Chthamalus stellatus distribution centers in the Mediterranean, reaching its northern limit in the Shetland Islands, north of Scotland.
At Millport, adults occur between mean high water levels of neap (M.H.W.N.) and spring tides (M.H.W.S.).
In southwest England and Ireland, Chthamalus are abundant when Balanus balanoides is scarce or absent (Southward and Crisp 1954, 1956).
Larvae settle from plankton mainly in September and October, with possible additional settlement until December.
Settlement is most abundant between M.H.W.S. and mean tide level (M.T.L.), on bare rock surfaces from mortality of Balanus, limpets, and other sedentary organisms.
Few Chthamalus that settle below M.H.W.N. survive, limiting adult presence at those levels.
Balanus balanoides is a boreal-arctic species, reaching its southern limit in northern Spain.
At Millport, it occupies almost the entire intertidal region, from mean low water of spring tides (M.L.W.S.) up to between M.H.W.N. and M.H.W.S.
Above M.H.W.N., it mixes with Chthamalus briefly.
Balanus settles on the shore in April and May, often densely.
The study's main goal was to determine why Chthamalus die below M.H.W.N.
Previous research showed physical conditions, space competition, and snail predation (Thais lapillus L.) are major mortality causes for Balanus balanoides.
Observations and experiments aimed to detect these factors' effects on Chthamalus survival.
Methods for Studying Barnacle Survival
Intertidal barnacles are ideal for studying survival in natural conditions due to their sessile nature, allowing direct observation of mapped individuals' survival.
Their small size and dense concentrations on exposed rocks make experimentation feasible.
They can be handled and transplanted on rock pieces without harm, as opercular plates close when exposed to air.
The experimental area was on the Isle of Cumbrae in the Firth of Clyde, Scotland, at Farland Point.
Farland Point, the island's southeast tip, faces moderate wave action.
The shore rock is old red sandstone, arranged as ridges oriented at right angles to the shoreline.
Connell (1961) provides a detailed description.
Other barnacle species present: Balanus crenatus Brug and Verruca stroemia (O. F. Muller), found in small numbers at and below M.L.W.S.
Measuring Chthamalus survival involved mapping individual positions in a patch.
Empty or missing barnacles at subsequent examinations were considered dead, as emigration is impossible.
Mapping: Thin glass plates (lantern slide cover glasses, , area ) were placed over barnacle patches, marking each Chthamalus' position with glass-marking ink.
Holes drilled in the rock marked plate corner positions.
Subsequent census observations were noted on paper copies of the glass map.
Study areas: Chthamalus patches were searched for below M.H.W.N. in a shore stretch of about 50 ft, stopping after finding 8 patches.
Rejection criterion: fewer than 50 Chthamalus in an area of about .
Each numbered area consisted of one or more glass maps in the area.
They were mapped in March and April 1954, before the main Balanus settlement in late April.
Very few Chthamalus settled below mid-tide level.
To study effects at lower levels, rock pieces with Chthamalus were moved from above M.H.W.N. to at and below M.T.L.
A hole was drilled through each piece and fastened to the rock with a stainless steel screw into a plastic screw anchor.
Hole dimensions: 1/4" diameter and 1" deep.
The screw could be repeatedly removed and replaced; only one stone was lost during the entire study.
For censusing, stones were taken to the lab during low tide for examination and returned before the tide rose.
Table I provides locations and arrangements of each area; transplanted stones are areas 11 to 15.
To study the effect of competition for space on Chthamalus survival: After Balanus settlement stopped in early June, reaching densities of on the experimental areas (Table I), a census of surviving Chthamalus was conducted on each area (Figure 1).
Each map was divided into two, aiming for roughly half the Chthamalus in each section.
Manipulating Balanus Density to Test Competition
One portion per map was chosen randomly (coin flip): Balanus touching or immediately surrounding each Chthamalus were carefully removed with a needle.
On the other portion, barnacles were left untouched.
This allowed measurement of the effect of intraspecific competition alone vs. competition with Balanus.
Equal numbers/densities of Chthamalus on the two sections of each area weren't possible, because Chthamalus often occurred in groups, requiring Balanus removal from around all group members to avoid crowding by Balanus.
Chthamalus densities were very low, so slight density differences between area portions probably didn't matter; intraspecific crowding was rarely seen.
Censuses of Chthamalus were every 4-6 weeks for the next year, noting factors like crowding, undercutting, or smothering since the last examination.
When necessary, Balanus that grew and threatened to touch Chthamalus were removed in later examinations.
Areas were located throughout the tidal range, either in situ or transplanted, to study effects of immersion (Table I). Area 1 had been under observation for 10 years.
Effects of wave shock differences couldn't be studied well in such a small area of shore, but any differences were noted in Table I.
To study effects of the predatory snail, Thais lapillus (synonymous with Nucella or Purpura, Clench 1947): Cages of stainless steel wire netting (8 meshes per inch) were placed over some areas.
This mesh has 60% open area; previous work (Connell 1961) showed it didn't inhibit barnacle growth or survival.
Cages were about 4x6 inches, with the roof about an inch above the barnacles, and sides fitted to the rock irregularities, held in place like the transplanted stones.
Transplanted stones were attached in pairs; one of each pair was caged (Table I).
These cages excluded all but the smallest Thais.
Occasionally, small Thais (1/2 to 1 cm long) entered cages through gaps where netting met the rock surface.
In concurrent Balanus study (Connell 1961), small Thais were estimated inside cages about 3% of the time.
All areas and stones were set up before Balanus settlement began in late April 1954.
Thus, Chthamalus on the shore were from the 1953 year class, about 7 months old.
Some Chthamalus that settled in autumn 1954 were followed until the study ended in June 1955.
Some adults, from their large size and eroded shells, must have settled in 1952 or earlier, were present on transplanted stones.
Records were kept of at least 3 year-classes of Chthamalus.
Results: Physical Factors Impact
Figures 2 and 3 show Chthamalus survival with and without Balanus contact (dashed line indicates survival without Balanus).
Suffix "a" indicates protection from Thais by a cage.
Without Balanus and Thais, and protected from water-borne objects, Chthamalus survival was good at all levels.
For those settled normally on the shore (Fig. 2), the poorest survival was on the lowest area, 7a.
On transplanted stones (Fig. 3, area 12), constant immersion in a tide pool resulted in the poorest survival.
Reasons for slightly greater mortality with increased immersion are unknown.
Algae amount on stones in the tide pool was much greater than on other areas, potentially reducing water/food flow or interfering with feeding.
Another indirect effect: increased snail predation (Thais lapillus) at lower levels.
Chthamalus is more tolerant of immersion than it normally experiences.
Shown by survival for a year on area 12 in a tide pool, and findings by Fischer (1928) and Barnes (1956a), who found Chthamalus withstood submersion for 12 and 22 months, respectively.
Its absence below M.T.L. might be due to lack of initial settlement or poor survival of newly settled larvae.
Lewis and Powell (1960) suggested increased light/warmth during emersion in early life on the shore favors Chthamalus.
These conditions would be more common higher on the shore in Scotland than in southern England.
Wave action effects on Chthamalus survival are hard to assess; like immersion, wave action may act indirectly.
Areas 7 and 12, with relatively poor survival, were also areas of least wave action.
Though Chthamalus is common on wave-beaten areas and absent from sheltered bays in Scotland, Lewis and Powell (1960) showed it can be very abundant in some sheltered bays.
Hatton (1938) found greater settlement and growth rates in wave-beaten areas at M.T.L. in northern France, but greater rates in sheltered areas at M.H.W.N..
At upper shore margins, Chthamalus exists higher than Balanus due to greater tolerance to heat and/or desiccation.
Evidence: Spring 1955.
Neap tides coincided with warm, calm weather in April.
For days, no water reached Area 1.
Between February and May censuses, one-year-old Balanus mortality was 92%, those 2+ years old, 51%.
Over the same period, Chthamalus mortality (7 months old) was 62%, those 10+ years old, 2%.
Records of Balanus survival below this showed only those in the top quarter of the intertidal zone suffered high mortality during this time (Connell 1961).
Competition for space impacts
At each census, notes were made of crowding events since the last census, detailing when one barnacle grew over another.
Intraspecific competition causing mortality in Chthamalus was rare.
In areas 2-7, on portions with Balanus removed, 167 deaths were recorded in a year.
Only 6 were due to crowding between Chthamalus.
On undisturbed portions, no such crowding was seen.
This aligns with Hatton's (1938) observation of rare Chthamalus crowding, unlike frequent Balanus crowding.
Interspecific competition between Balanus and Chthamalus was a major cause of Chthamalus death.
Shown by direct crowding process observations at each census and differences between survival curves of Chthamalus with and without Balanus.
From periodic observations on undisturbed portions of areas 3-7, after the first month:
About 10% of Chthamalus were covered by growing Balanus.
About 3% were undercut and lifted by growing Balanus.
A few died without crowding.
By the end of the second month:
About 20% of Chthamalus were wholly or partly covered by Balanus.
About 4% had been undercut.
Others were surrounded by tall Balanus.
These processes continued at a lower rate in the autumn and ceased during the later winter.
In the spring, Balanus resumed growth and more crowding was observed.
Table II summarizes these observations for undisturbed portions of all areas.
Above M.T.L., Balanus tended to overgrow Chthamalus, whereas at lower levels, undercutting was more common.
This trend was evident within each group of areas; undercutting was more prevalent on area 7 than on area 3, for example.
Faster Balanus growth at lower levels (Hatton 1938, Barnes and Powell 1953) may have resulted in more undercutting.
Chthamalus completely covered by Balanus were recorded as dead, even if death wasn't immediate.
Table II defines "other crowding" as instances of Chthamalus being crushed laterally between Balanus or disappearing amid dense Balanus growth.
Area 7a: High Balanus density (48 per ) limited expansion except upward, leading to tall cylindrical/conical barnacles.
Comparing survival curves (Figs. 2 and 3) within each area shows Chthamalus free of Balanus survived better than those in undisturbed areas on all but areas 2 and 14a.
Area 2: Balanus and Chthamalus adults normally mix; Balanus has no influence on Chthamalus survival.
Stone 14a: Chthamalus survival without Balanus was better until January, when a starfish (Asterias rubens L.) entered the cage and ate the barnacles.
Much variation occurred on the other 14 areas.
When Chthamalus without Balanus are compared to those on adjacent undisturbed area portions, survival was better on 10 areas and moderately better on 4.
In undisturbed portions, some Chthamalus escaped severe crowding.
Sometimes no Balanus settled close to a Chthamalus, or those that did died soon after settlement.
Some Chthamalus being undercut by Balanus attached themselves to the Balanus and survived.
Some Chthamalus were partly covered by Balanus but still survived.
Areas 4, 6, 11a, and 11b: Chthamalus survived well in Balanus presence, likely escaping death in one of these ways.
Detailed tracking of young Chthamalus settling in autumn 1954 on stone 15 and area 7b.
Chthamalus on stone 15 settled in an irregular space surrounded by large Balanus.
Most mortality occurred around space edges as Balanus undercut nearby small Chthamalus.
Mortality of Young Chthamalus by Crowding (Stone 15 between Sept 30, 1954 and Feb 14, 1955)
Lifted by Balanus: 29
Crushed by Balanus: 4
Smothered by Balanus and Chthamalus: 2
Crushed between Balanus and Chthamalus: 1
Lifted by Chthamalus: 1
Crushed between two other Chthamalus: 1
Unknown: 3
Crowding of newly settled Chthamalus by older Balanus in autumn mainly takes the form of undercutting, not smothering as in spring.
In spring, Chthamalus are more firmly attached, so fast-growing young Balanus grow over them upon contact.
In autumn, Balanus are firmly attached, Chthamalus weakly so.
Chthamalus settlement was very dense, , on Stone 15, so they mostly touched each other, but only 2 of 41 deaths were due to intraspecific crowding.
This agrees with findings from the 1953 settlement of Chthamalus.
Mortality rates for young Chthamalus on area 7b showed seasonal variations.
Between October 10, 1954 and May 15, 1955, the relative mortality rate per day was 0.14 on the undisturbed area and 0.13 where Balanus had been removed.
Over the next month, the rate increased to 1.49 on the undisturbed area and 0.22 where Balanus was absent.
Thus, increased mortality of young Chthamalus in late spring was also associated with Balanus presence.
Some stones transplanted from high to low levels in spring 1954 bore adult Chthamalus.
Survival of these adults, from autumn 1952 or earlier, at least 20 months old at experiment start, was recorded on 3 stones.
Mortality was much greater when Balanus was not removed (Table III).
On 2 of 3 stones, mortality was almost as high as that of the younger group, suggesting any Chthamalus surviving competition with Balanus during the first year would be eliminated in the second year.
Balanus censuses weren't made on experimental areas; survival was being studied on other areas in the same shore stretch during the same period (Connell 1961).
Mortality rates measured in that study are listed in Table IV; Balanus were from the 1954 settlement at similar population densities and shore levels to this study.
Balanus mortality rates were about the same as those of Chthamalus in similar situations except at the highest level, area 1, where Balanus suffered much greater mortality than Chthamalus.
Most of this mortality was caused by intraspecific crowding at all levels below area 1.
Observations at each census indicated Balanus was growing faster than Chthamalus.
Growth rates of the two species were measured from photos taken in June and November 1954 (Table V).
Balanus growth rate was greater than Chthamalus in experimental areas, agreeing with Hatton's (1938) findings on the French shore and Barnes' (1956a) for continual submergence on a raft at Millport.
After a year of crowding, average Balanus and Chthamalus population densities remained proportionally the same as at the start, since mortality rates were similar.
However, because of its faster growth, Balanus occupied a relatively greater area and likely had greater biomass compared to Chthamalus after a year.
Faster Balanus growth explains how they crowded Chthamalus and the sinuosity of Chthamalus survival curves growing in contact with Balanus.
Mortality rate of these Chthamalus (slope of curves in Figs. 2 and 3) was greatest in summer, decreased in winter, and increased again in spring.
Survival curves of Chthamalus growing without Balanus contact don't show these seasonal variations, so they can't be due to physical factors like temperature, wave action, or rain.
Seasonal variations in Balanus growth rate correspond to these changes in Chthamalus mortality rate.
Figure 4 compares Balanus growth throughout the year (Barnes and Powell 1953) to Chthamalus survival at about the same intertidal level in this study.
Increased Chthamalus mortality occurred in the same seasons as increases in Balanus growth rate.
Correlation tested using Spearman rank correlation coefficient.
Absolute increase in diameter of Balanus each month, from growth curve, was compared to percentage mortality of Chthamalus in same month.
For the 13 months with available data, the correlation was highly significant, .
All these observations suggest poor Chthamalus survival below M.H.W.N. is mainly due to crowding by dense Balanus populations.
At experiment end in June 1955, surviving Chthamalus were collected from 5 areas.
Table VI shows the average size was greater in Chthamalus that had grown free of Balanus; the difference was significant (P < .01, Mann-Whitney U. test, Siegel 1956).
Survivors on undisturbed areas were often misshapen, sometimes from being lifted onto the side of an undercutting Balanus.
Smaller size of crowded barnacles may be due to disturbances in normal growth patterns while being crowded.
Chthamalus were examined for developing larvae in their mantle cavities.
Table VI indicates that in every area, the proportion of uncrowded Chthamalus with larvae was equal to or slightly greater than in crowded areas.
This may relate to the smaller size of crowded Chthamalus and isn't due to separation, since Chthamalus can self-fertilize (Barnes and Crisp 1956).
Moore (1935) and Barnes (1953) showed that the number of larvae in Balanus balanoides increases with parent volume.
Comparing the cube of diameter (proportional to volume) of Chthamalus with and without Balanus, volume can decrease to 1/3 normal size when crowding occurs.
Assuming a similar relation between larval numbers and volume in Chthamalus, competition with Balanus decreases both the frequency and abundance of larvae in Chthamalus.
This satisfies both aspects of interspecific competition (Elton and Miller 1954): One species affects another by interference, i.e., reducing reproductive efficiency or increasing mortality of its competitor.
Predation impact by Thais
Cages excluding were placed on 6 areas (
Predation impact by Thais
Cages excluding Thais were placed on 6 areas (Table I) in April 1954.
At the two highest levels (areas 1a and 2a), cages had no significant effect on Chthamalus survival (Fig. 2).
Thais is scarce at this level, so lack of a significant effect is unsurprising.
Below this level, cages greatly increased Chthamalus survival over about 8 months but had little or no effect during the last 3 months, especially on undisturbed portions of areas 3a, 4a, 5a, and 6a.
Cage roof was about 1 inch above the barnacles.
Uncaged barnacles grew to this height within 8 months, and Thais could prey upon them by reaching under the cage sides, especially in the undisturbed portions where barnacles were taller and more crowded.
Cage effectiveness also decreased with time due to the increasing size of Thais inside.
Small Thais that entered through the meshes and gaps grew, becoming large enough to prey effectively on Chthamalus.
Despite decreased cage effectiveness, predation losses were considerable on areas 3-6.
Figure 5 compares Chthamalus survival on the undisturbed portions of caged and uncaged areas.
Greatest predation effect: area 6, lowest level in this group (4-7).
Area 7 was lower than all the caged areas, and survival dropped to zero by February 1955.
High mortality can't be attributed solely to predation; crowding by Balanus was also significant.
Area 14: Stones transplanted to M.T.L. from above M.H.W.N. to study individual factor effects, had both competition and predation act strongly.
On stone 14, Chthamalus survived well without Balanus (Fig. 3), until a starfish entered the cage in January 1955 and ate all the barnacles.
On stone 14a without a cage, predation occurred throughout the experimental period, and few barnacles survived by January 1955.
Area 15: No cage was present, but Balanus was removed to allow greater Thais access.
Chthamalus mortality was greater than at any other level but was similar in pattern to area 6, suggesting Thais impact was also important at this level.
Predation was probably less intense on some areas due to fewer Thais being present; the snail population varied greatly along the shore due to irregular rock arrangements.
Snail density was studied (Connell 1961), but no reliable measures of local density were made at the experimental areas.
However, observations suggest area 5 had a lower snail population than areas 3, 4, and 6, possibly explaining slightly better Chthamalus survival on area 5.
Presence of the dog whelk, Nucella lapillus, is influenced by the roughness of the shore and the abundance of food (barnacles and mussels).
Sheltered shores and those with high barnacle densities tend to have larger populations of Nucella lapillus.
Predation by Thais may be more important in determining the lower limit of Chthamalus than previously thought.
Discussion on Barnacle Distribution Factors
Chthamalus upper limit is controlled by its greater resistance to heat and desiccation than Balanus, as shown by the 1955 spring tide observations.
Chthamalus lower limit is controlled by a combination of factors:
Competition for space with Balanus.
Predation by Thais.
Possibly other physical factors like wave action or light.
Competition occurs through direct crowding during the rapid growth of Balanus in spring and summer.
Predation occurs mainly at lower levels where Thais is more abundant and can limit Chthamalus survival even when competition from Balanus is reduced.
Physical factors may influence Chthamalus survival indirectly by affecting the growth rates and competitive ability of Balanus or the foraging behavior and abundance of Thais.
Chthamalus is more tolerant of immersion than it normally experiences, as indicated by its survival in tide pools and laboratory experiments.
It's absence below M.T.L. is likely due to biotic factors rather than its physiological inability to survive when submerged.
Southern distribution: Chthamalus is more abundant in southwest England and Ireland when Balanus is scarce or absent (Southward and Crisp 1954, 1956).
Likely due to the absence of intense competition with Balanus.
In the Mediterranean, competition from Balanus is less intense, and predation pressure may be lower, allowing Chthamalus to thrive.
Balanus populations are limited by a parasite (Acanthochitona fascicularis), allowing Chthamalus to flourish in the Mediterranean (Barnes, 1958).
Relative importance of competition and predation depends on local environmental conditions, barnacle recruitment rates, and predator densities.
These local biotic interactions play a crucial role in determining species distribution patterns in marine intertidal communities.
The study highlights the complex interplay of biotic and abiotic factors shaping species distribution patterns.
The importance of considering multiple interacting factors rather than single explanations when investigating ecological phenomena is also highlighted.