Journal of Experimental Marine Biology and Ecology 330 (2006) 482–492 www.elsevier.com/locate/jembe
Effects of competition on an endangered limpet Patella ferruginea (Gastropoda: Patellidae): Implications for conservation
Free Espinosa a,*, Jose´ M. Guerra-Garcı´a a, Darren Fa b, J. Carlos Garcı´a-Go´mez a
a Laboratorio de Biologı´a Marina. Facultad de Biologı´a. Avda. Reina Mercedes 6, 41012 Sevilla, Spain b Gibraltar Museum, 18-20 Bomb House Lane, Gibraltar, UK Received 20 April 2005; received in revised form 16 September 2005; accepted 16 September 2005
Abstract
Spatial and trophic competitive interactions were analysed for the seldom-studied limpet Patella ferruginea (which is considered as an bextinction riskQ). Spatial patterns of distribution of P. ferruginea were studied using quadrats of 1 1m2 at several transects along the coastline, whereas trophic interactions were studied through manipulations of densities of P. ferruginea and Patella caerulea in experimental plots located at the mid-shore. Physical parameters were measured inside each plot to determine the microenvironmental differences between fenced and unfenced plots. Fenced plots of 50 50 cm2 were used with six different treatments. Mortality was recorded every 15 days and length was measured monthly during the 3.5 months of the experiment. At the beginning and end of the experiment, lengths and weights of limpets were recorded and chlorophyll concentration was measured by spectrophotometric analysis of rock surface. Both species showed increased mortality and reduced size and weight in treatments with greater densities. High intraspecific competition was detected in P. caerulea compared with P. ferruginea whereas asymmetrical interspecific competition was observed. The results suggest that P. caerulea is the superior competitor, possibly due to differences in radular morphology and mobility between the two species. Microalgal food assessment showed that it is probably a limiting resource, especially for P. caerulea, although this species has a lower biomass than P. ferruginea. The high intraspecific competition observed in P. caerulea could be responsible for the coexistence of both species. The present study may be useful in helping to conserve P. ferruginea, which is presently under serious threat of extinction, because the results show that experimental fences are a viable means of concentrating breeding individuals. D 2005 Elsevier B.V. All rights reserved.
Keywords: Competition; Intertidal; Limpets; Patella caerulea; Patella ferruginea; Translocation
1. Introduction Competition on rocky shores is of three general types, namely pre-emptive competition, interference A two-dimensional space is a resource required by competition or exploitative competition (see Under- almost all intertidal rocky shore species, either directly wood, 2000) where several species need the same as an absolute need for space on which to settle and space to feed; however, there is insufficient food to grow or as a relative need for space over which to feed support all the animals needing it (e.g. Underwood, (Underwood, 2000). 1984). Of these, exploitative competition is often ob- served within phyla, since closely related species usu- * Corresponding author. Tel.: +34 954234904. ally have the greatest overlap in the resources they E-mail address: [email protected] (F. Espinosa). require, and are more likely to compete if they are
0022-0981/$ - see front matter D 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2005.09.020 F. Espinosa et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 482–492 483 coexistent. In limpets, food and space are the major greatest densities of P. ferruginea in this area, similar resources competed for (Branch, 1975a). Furthermore, to other places in the Mediterranean with well estab- competition among and within species of limpets for lished populations (Guerra-Garcı´a et al., 2004). Both food is a widespread and normal aspect of the ecology species are distributed from the mid to the upper of limpets (see Underwood, 2000). Due to their mobil- littoral. Other species present were Cymbula safiana ity, grazers that encounter a food shortage in one local- Lamarck, 1819, Patella ulyssiponensis Gmelin, 1791, ity can move to other areas where food is more Patella rustica Linnaeus, 1758 and Siphonaria pecti- abundant. Space at any level of the shore provides a nata (Linnaeus, 1758). The first two inhabit the low place for limpets to live and food to eat (Frank, 1965; littoral/sublittoral, whereas P. rustica inhabits the Sutherland, 1970). Several studies have shown that in upper intertidal zone (Sella et al., 1993; Fa, 1998, such circumstances the presence of one species may personal observation). Thus, these three species of have profound and quantifiable effects on another Patella have different zonation patterns from P. ferru- (Black, 1979; Creese and Underwood, 1982; Ortega, ginea and are unlikely to compete with it. In the case 1985; Iwasaki, 1993). Manipulative experiments which of S. pectinata, its zonation is similar to P. ferruginea. prevent emigration with the use of enclosures indicate However, pulmonate limpets have no detrimental that competitive interactions among herbivorous gastro- effects on prosobranch limpets due to their weak rad- pods result in increased mortality, decreased shell ular structure (Black, 1979; Creese and Underwood, growth and reduced tissue mass (Haven, 1973; Under- 1982; Ortega, 1985; Iwasaki, 1993; Ocan˜a and Fa, wood, 1976, 1978, 1984; Creese and Underwood, 2003). Therefore, the single species that could have 1982; Fletcher and Creese, 1985; Ortega, 1985; a significant influence on P. ferruginea would be P. Quinn and Ryan, 1989; Lasiak and White, 1993). caerulea, and, for this reason, we focused the present The limpet Patella ferruginea Gmelin, 1791, en- study on competitive interactions between these two demic to the Mediterranean, is the most endangered species. invertebrate marine species on the list of the European Natural densities of P. caerulea in the Strait of Council Directive 92/43/EEC on the conservation of Gibraltar area have been quantified by Ocan˜a (1997) Natural Habitats and of Wild Fauna and Flora, 1992 as 125 individuals/m2. In the breakwater under study, requiring bstrict protectionQ (Ramos, 1998), and it is, similar densities of around 100 individuals/m2 have presently, under serious risk of extinction (Laborel- been observed (unpublished data). Additionally, the Deguen and Laborel, 1991a; Templado and Moreno, mean density of P. ferruginea along linear transects 1997; BOE, 1999), whereas Patella caerulea Linnaeus, has been estimated as 1.13 individuals/m inside the 1758, is the common Mediterranean limpet. harbour of Ceuta (Guerra-Garcı´a et al., 2004), reaching The aim of the present study was to explore the more than 2 individuals/m in some areas (unpublished competitive interactions on the endangered limpet P. data). We have used a dcontrol densityT of 2 individuals ferruginea and its interspecific relationships with P. per plot (8 individuals/m2)ofP. ferruginea (see Section caerulea, considering that little is known about the 2.3.2) based on the requirements for subsequent statis- biology of the species (Guerra-Garcı´a et al., 2004) tical analyses, and taking into account that the biomass and taking into account that P. caerulea overlap its of the two species is quite different, the use of the same niche with P. ferruginea. An effective management number of individuals of each species is not a reliable program, when transfer operations are required by re- method because, in this case, the biomass of P. ferru- population of areas or by threat of engineering building, ginea would be much higher than P. caerulea. could be developed under the results of the present study. 2.2. Physical parameters
2. Material and methods To characterise the influence of the experimental enclosures on the physical environment of limpets, 2.1. Site and species studied measurements of temperature, humidity and irradiation were taken inside each plot over the rock on every The study was carried out along a breakwater locat- sampling occasion (N =120 for each parameter). A ed inside the harbour of Ceuta (35853V20WN/ digital thermometer for temperature, a hygrometer 5818V30WW), on the coast of North Africa in the Strait (Hanna Higrocheck HI98601n ) for humidity and lux- of Gibraltar. The studied species were Patella ferrugi- ometer (Gossen Mavolux 5032C n ) for irradiation were nea and Patella caerulea. Ceuta’s harbour has the used. 484 F. Espinosa et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 482–492
2.3. Experiments to determine the effects of inter- and 2.3.2. Trophic intra- and interspecific competition on P. intraspecific competition ferruginea and P. caerulea Inter- and intraspecific competitive interactions were 2.3.1. Spatial competition in P. ferruginea analysed through an experimental manipulation of den- A total of 11 horizontal linear transects of 50 m were sities of adult animals of the most frequent sizes: 20–30 placed parallel to the shore, one every 2 km along the mm for P. caerulea and 40–50 mm for P. ferruginea coastline of Ceuta. A quadrat of 1 1m2 was placed on (unpublished data), in different mixtures of the two the substrate and the individuals present were registered; species in fenced enclosures. We used a control density the quadrat was moved along the transect until 50 mea- (natural density) vs. high density (quadruple) of the sures were obtained. The variance/mean quotient was same and the other species, in a total of 6 treatments calculated with all data obtained from plots of all trans- (Table 1). This type of asymmetrical design was used in ects, since according to Margalef (1974), this quotient is this experiment because inter- and intraspecific com- very useful to determine the type of distribution of the petitive interactions need to be investigated simulta- organisms. At the same transects, the distance separating neously (Underwood, 1992). Three replicates of each nearest-neighbours limpets and their shell sizes were treatment were randomly allocated to the plots. Plastic- measured. This method for inferring competition be- coated wire fences, with a square mesh of 10 10 mm, tween coexisting limpets was used by Black (1979). were used to enclose the limpets inside the plots of Shell lengths were measured to the nearest mm with 50 50 cm. The fences were attached to the rock by calipers and distance between nearest neighbours was stainless steel screws inserted into raw-plugs in holes measured to the nearest mm using a tape measure to and closed at their top using the same mesh. By closing follow the rock profile. Once measurements had been the tops, we avoided the influence of predation. To test recorded for a particular pair of limpets, they were the effect of the fences on adult animals, which can excluded from further analyses. This process was con- forage over a larger area than that enclosed by the tinued until measurements for 98 pairs were obtained. To experimental plot, unenclosed control animals were test the accuracy of the results obtained with the method also used. This consisted of monitoring the same num- of Margalef (1974) on distributional patterns, we have ber of animals (three sets of two limpets for P. ferrugi- also used the formulation developed by Clark and Evans nea and twenty-five for P. caerulea) in open areas of (1954) which quantifies the pattern of dispersal. Their the shore. dispersal coefficient (R) is calculated as follows: The experiment ran for 14 weeks between July and X October 2004. On every sampling occasion, the fences pffiffiffi R ¼ r=N 2 p were checked and repaired. The limpets that died were replaced with new ones that matched the size of the where r =distance between each animal and its nearest missing limpets and marked with epoxy resin Eporai neighbour, N =number of animals and p =density 1127n to distinguish them from the original limpets. (where area is measured in the same units as distance). The data collected in each monitoring date and pre- We used as density the mean of all transects sampled. sented in the results refer always and only to the Values of 0, 1 and 2 for R correspond to complete original animals when the experiment was started. aggregation (contagious behaviour), random distribu- The number of surviving limpets was recorded every tion and perfect (uniform) dispersal, respectively. 15 days and their total shell lengths were read at
Table 1 Experimental treatments and total number of limpets per fence Treatments Number of limpets per enclosure Mean biomass per individualFS.D. (g) Total biomass per treatment (g) Intraspecific interactions C1D (control) 25 C 1.85F0.53 46.25 F1D (control) 2 F 12.36F3.71 24.72 C4D (increased 4) 100 C 1.72F0.7 172 F4D (increased 4) 8 F 10.19F3.51 81.52
Interspecific interactions C4D+F1D 100 C+2 F 1.69F0.62+8.36F1.55 169+16.72 F4D+C1D 8 F+25 C 10.32F3.5+1.81F0.7 82.56+45.25 C=P. caerulea;F=P. ferruginea; D=density. F. Espinosa et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 482–492 485
Table 2 trols. Kolmogorov–Smirnov and Levene tests were F Physical parameters (mean S.D.) on fenced and unfenced experi- used to determine normality and homogeneity of var- mental treatments iances, respectively. Exponential and logarithmic trans- Temperature (8C) Humidity (%) Irradiation (lx) formations were necessary to meet the assumption of Fenced 22.04F1.66 77.11F4.58 31048F17807 normality and homogeneity of variances. F F F Unfenced 23.85 2.16 73.18 6.17 68876 16891 The effects of inter- and intraspecific competition on F 22,62*** 13,74*** 104,09*** 1,118 proportional mortality, length, weight and chlorophyll Value of the ANOVA test. concentration during the experiment were also analysed *** p b0.001. with ANOVA test. Absolute values of proportional mortality and chlorophyll per replicate were used in monthly intervals, in situ with calipers, without remo- the analysis. In the case of analysis of length and ving the animals. At the end of the experiment, after weight, however, each value corresponded to the aver- approximately 3.5 months, all the remaining original age of all limpets in the replicate. When significant limpets were collected, and their lengths and wet differences were found among treatments, post hoc weights were recorded. Lengths and weights of the pairwise comparisons on length and weight were car- original limpets were also measured at the beginning ried out. Tukey’s test was used for post hoc compar- of the experiment. Individual marking was not possible isons. Physical parameters were compared between all and the measurements were always treated as averages fenced and unfenced plots to observe differences in the per plot. physical environment using ANOVA test. Statistical analyses were carried out with SPSSn 12.0. 2.4. Microalgal food assessment 3. Results To assess the influence of different densities of grazing limpets on microalgal abundance, the chloro- 3.1. Physical parameters phyll concentration of the substratum was estimated. At the beginning and end of the experiment a surface The physical environment was significant different of 10 10 cm2 was brushed with a stiff toothbrush between fenced and unfenced treatments (see Table 2), within each enclosure and the resulting slurry was with greater values of temperature and irradiation and treated with 20 ml of 100% methanol to extract the lower values of humidity in the unfenced plots than in pigments. The samples were frozen and maintained in the fenced ones. Consequently, physical stress inside darkness until analysis (minimum of 24 h). Finally, the fenced experimental plots was lower. samples were filtered through a Whatman GF/C filter and the measurements of absorbance were carried out 3.2. Spatial competition with a spectrophotometer (Pharmacia Biotech Novas- pec IIn). The chlorophyll concentration was calcula- Observations in the field seem to indicate that P. ted according to the formula of Thompson et al. ferruginea individuals do not space themselves out (1999). with respect to conspecifics, since in some cases their
½ ¼chlorophyll a 13:0 A665 v=ðÞd V 120 where 13.0=constant for methanol, A665 =net absor- bance of solution at 665 nm, v =final volume of 100 r = 0,0063 ns solution (20 ml), d =path length of cell (1.6 cm), 80 2 V =surface area of sample (100 cm ). 60
2.5. Data analysis 40 Distance (cm) 20 Single-factor analyses of variance were used to test 0 the influence of experimental enclosures on proportion- 0 5 10 15 20 al mortality (the sum of original animals dying over the Sum of shell sizes (cm) 14 weeks/number of limpets in the treatment), length, Fig. 1. Scattergraph showing the relationship between the sum of shell weight and variation of chlorophyll concentration dur- sizes and distance apart of nearest neighbours for Patella ferruginea. ing the experiment, between unfenced and fenced con- Pearson’s correlation coefficient is noted; ns=not significant. 486 F. Espinosa et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 482–492
Table 3 Mean (FS.D.), ANOVA tests and p values between fenced and unfenced controls for the studied parameters Fenced control vs. Patella caerulea Patella ferruginea Unfenced control Fenced mean Unfenced mean Fk 1,n k p Fenced mean Unfenced mean Fk 1,n k p (FS.D.) (FS.D.) (FS.D.) (FS.D.)
Proportional mortality 0.09 (0.06) 0.58 (0.22) 13,1631,4 0.022* 0 (0) 0.33 (0.28) 41,4 0.116 ns Mean shell length (mm) 28.51 (2.39) 28.87 (3.66) 0,1511,97 0.698 ns 57.5 (3.33) 57.7 (4.03) 0,0121,8 0.917 ns Mean wet weight (g) 2.99 (0.75) 2.87 (1.09) 0,0111,97 0.916 ns 21.95 (6.11) 22.25 (5.39) 0,0061,8 0.939 ns 2 D Chlorophyll (Ag/cm ) 0.02 (0.16) 0.04 (0.11) 0,8041,4 0.421 ns 0.203 (0.16) 0.14 (0.16) 0,2031,4 0.676 ns ns=not significant. * p b0.05. shells appeared to be actually in contact. The low The study of spatial distribution of the individuals of correlation coefficient obtained between the sum of P. ferruginea showed an aggregational pattern (S2/ shell sizes and the distance apart of nearest neighbours l =2.5484; p b0.05; N =550), according to the graphi- supports this contention (Fig. 1). cal scattergraph of Margalef (1974). Moreover, the
Patella caerulea Patella ferruginea Intraspecific interactions
ab1D 4D 1D 4D
100 10
80 8
60 6
40 4
Mean number of 20 2 live limpets remaining 0 0 0 153045607590105 0 15 30 45 60 75 90 105 Interspecific interactions
c d C1D C1D-F4D C4D-F1D F1D F1D-C4D F4D-C1D
9 120 8 100 7 6 80 5 60 4 40 3 2
Mean number of 20 1
live limpets remaining 0 0 0 153045607590105 0 153045607590105 Days from start of experiment
Fig. 2. Mean number of live limpets remaining (FS.D.) in the experimental treatments. F. Espinosa et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 482–492 487 value of the coefficient from Clark and Evans (1954) and the relatively small number of individuals per plot, was 0.30, confirming the result obtained with the meth- since the p-value was clearly lower than for the other od of Margalef (1974). parameters.
3.3. Effects of confinement 3.4. Mortality
The fencing procedure did not seem to affect mean The mean number of limpets that remained alive in chlorophyll concentration or shell length or weight of P. control treatments declined very slightly during the caerulea or P. ferruginea, as no significant differences experimental period for P. caerulea, whereas for P. were obtained between fenced and unfenced controls ferruginea, not a single specimen died (Fig. 2a, b). In (Table 3). Mortality, however, was higher in unfenced contrast, mortality on P. caerulea was much greater than fenced controls (Table 3), which may be related to (about 30%) with increased density ( 4), whilst P. a dprotective effectT of experimental plots against pre- ferruginea showed no density dependence. In two-spe- dators and physical stress. However, the differences cies combinations, P. caerulea did not show important were significant for P. caerulea only. Although a non- effects on mortality, when held with P. ferruginea,but significant value was obtained for P. ferruginea,it when its own density was increased, again the mortality could be a consequence of the low power of this test was great (around 30%) (Fig. 2c). There were no sig-
Patella caerulea Patella ferruginea Intraspecific interactions a b C1D C4D F1D F4D
35 65
60 30 55
50 25 45 Mean shell length (mm) 20 40 03060105 03060105 Interspecific interactions c d C1D C4D-F1D C1D-F4D F1D F4D-C1D F1D-C4D
35 65 60 55 30 50 45 25 40 35
Mean shell length (mm) 20 30 0 30 60 105 0 30 60 105 Days from start of experiment
Fig. 3. Mean shell length (FS.D.) during the experimental period. 488 F. Espinosa et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 482–492 nificant differences in mortality for P. caerulea among Table 5 Pairwise comparisons for Patella caerulea treatments ( F3,8 =1,43; p =0.302). On the other hand, P. ferruginea showed clear increases in mortality when Comparison Significance P. caerulea was added, around 35% in the presence of Length Weight quadruple densities and 30% in the presence of control C1D vs. densities of P. caerulea, respectively (Fig. 2d), although C4D p b0.001 p b0.001 no significant differences were obtained among treat- C1D F4D p b0.001 p b0.001 b b ments for P. ferruginea ( F =1,86; p =0.213). C4D F1D p 0.001 p 0.001 3,8 C4D vs. C1D F4D ns ns 3.5. Growth C4D F1D p b0.001 p b0.001 C1D F4D vs. Mean shell length increased markedly over the ex- C4D F1D ns p b0.001 perimental period, especially in control treatments (Fig. ns=not significant. 3a,b). Significant differences were observed in P. caer- ulea ( F3,535 =30,88; p b0.001) and P. ferruginea 3.6. Weight ( F3,46 =16,7; p b0.001) among treatments, by the end of the experiment. After 30 days, P. caerulea ceases the In control densities of both species, weight was increase in growth in C4D treatment, whereas P. ferru- much greater at the end of the experiment compared ginea continues growing in F4D treatment, showing with the results for increasing densities, indicating greater intraspecific competition in the former species. strong intraspecific competition on both species. How- Growth was significantly lower in increased density ever, in two-species combination, the negative effect on treatments compared with control treatments for both final weight after the experimental period was much species (Tables 4 and 5). The interspecific interactions more pronounced on P. ferruginea than on P. caerulea showed that P. caerulea was more affected at high (Fig. 4a,b). P. ferruginea lost weight in the presence of densities, whereas a weaker effect on growth was high densities of P. caerulea whereas P. caerulea in- detected in the presence of high densities of P. ferrugi- creased in weight even when P. ferruginea was at high nea (Fig. 3c). The same pattern was observed for densities. Significant differences were found among proportional mortality, indicating that intraspecific treatments at the end of the experiment for P. caerulea interactions are stronger in P. caerulea than interspe- ( F3,535 =50,65; p b0.001) and P. ferruginea ( F3,46 = cific ones. 11,36; p b0.001). Increasing densities significantly re- For P. ferruginea, a practical absence of growth was duced the weight of the limpets in intraspecific treat- observed in the presence of P. caerulea at high densities ments (Tables 4 and 5) for both species. However, for (Fig. 3d), whilst the presence of P. caerulea at control interspecific treatments, high densities of P. caerulea densities produced lower growth that only high density resulted in a significant weight decrease in P. ferrugi- of P. ferruginea (46.29 mm vs. 49.6 mm of mean shell nea when compared with the control densities of the length at the end of the experiment), indicating that the other species (Table 4), although P. ferruginea was at presence of P. caerulea has a strong negative effect on quadruple densities. In contrast, P. caerulea showed a P. ferruginea. significant increase in weight in the presence of high densities of P. ferruginea when compared with the Table 4 treatment C4D+F1D, indicating that the presence of Pairwise comparisons for Patella ferruginea P. ferruginea was not decisive but not so the increase in Comparison Significance density of the own species (Table 5). Length Weight F1D vs. 3.7. Microalgal food F4D p b0.001 p b0.01 F1D C4D p b0.001 p b0.001 No significant differences were found between the F4D C1D p b0.001 p b0.001 beginning and end of the experiment in chlorophyll F4D vs. b b concentration, except for treatment F1D ( F1,4 =10,94; F1D C4D p 0.05 p 0.05 b F4D C1D p b0.05 ns p 0.05) (Fig. 5). Significant differences were detected F1D C4D vs. in chlorophyll concentration among different treatments F4D C1D ns ns at the end of the experiment ( F5,12 =4,73; p b0.05) due ns=not significant. to an increase in chlorophyll concentration in treatment F. Espinosa et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 482–492 489
a phyll concentration. Nevertheless, high densities of 30 limpets did not produce the complete depletion of
(g) Initial 25 End food resources. 20 15 4. Discussion 10 4.1. Competitive interactions 5 Mean wet weight of Patella ferruginea 0 Many studies have been conducted to explore com- F1D F4D F1D- F4D- C4D C1D petitive interactions through quantitative experimental Treatments manipulations on distantly related species (Dayton, b 1971; Underwood, 1978,1984; Ortega, 1985; Iwasaki, 4 Initial 1993). Much less work has been done on closely related 3,5 (g) End species (see Branch, 1975b and Boaventura et al., 2002). 3 2,5 Pielou (1962) and Yeaton and Cody (1976) sug- 2 gested that evidence for competition for space exists 1,5 when nearest neighbour distances are greater for larger 1 individuals than smaller. On these grounds, intraspecif- 0,5 ic space competition in P. ferruginea appears quite low, Mean wet weight of Patella caerulea 0 since no significant correlation was obtained between C1D C4D C1D- C4D- F4D F1D distance separating nearest neighbours and their shell Treatments sizes. Additionally, the aggregating behaviour observed probably shows low intraspecific spatial competition Fig. 4. (a) Changes in mean wet weight for Patella ferruginea at the because if high competition exists the species would start and end of the experiments for all treatments. (b) Changes in have a random or dispersed pattern, as proposed by mean wet weight for Patella caerulea at the start and end of the experiments for all treatments. Branch (1975b) who pointed out that intraspecific com- petition intensity will decrease in limpet species which are sparsely distributed. F1D. This increase was associated with a significant P. ferruginea lives high on the shore, within the increase in both length and weight of P. ferruginea. upper midlittoral (Pe´res and Picard, 1964; personal Additionally, an important decrease in chlorophyll in observations) where desiccation and temperature quadruple density treatments compared with control changes are assumed to be limiting (see Little and ones was observed (Fig. 5), and lower values of growth Kitching, 1996) and aggregation could be a response and weight gain were achieved for both species in these to desiccating conditions as pointed out by Branch cases, as well as for treatment C4D F1D when com- (1975b) from several studies on limpets (Abe, 1931; pared with treatment F4D C1D with higher chloro- Frank, 1965; Millard, 1968; Breen, 1972).
0,45 * p<0.05 0,4 0,35 Initial End
) 0,3 2 0,25
g/cm 0,2 µ ( 0,15 Chlorophyll a 0,1 0,05 0 C1D C4D C4D-F1D F1D F4D F4D-C1D Treatments
Fig. 5. Mean chlorophyll concentration (FS.D.) at the beginning and end of the experiment. *Treatment with significant differences at p b0.05 between initial and end of the experiment. 490 F. Espinosa et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 482–492
Most studies of competition have shown asymmet- et al. (2002) did not find evidence that exploitation of rical interspecific interactions (see Connell, 1983) in- resources was the direct cause of reduced survivorship, cluding those on limpets (Black, 1979; Creese and length, weight and fecundity with increasing densities, Underwood, 1982; Ortega, 1985; Iwasaki, 1993). How- although at background densities, resources were limit- ever, these studies were focussed between pulmonate ing. In the present study, food supply decreased signif- and prosobranch limpets, with different grazing abilities icantly with increases in limpet densities, and could be a due to their different radular structures (see Lasiak and factor limiting the growth and weight of both species White, 1993). When species with similar radula were studied. Similar studies also conducted in the area of the tested, symmetrical interspecific interactions appeared Gibraltar Strait on Siphonaria pectinata and P. caerulea (Boaventura et al., 2002). In the present study, some interactions showed that when the amount of food avail- asymmetrical interactions could be occurring, since P. able for a species is greater, then competitive effects are ferruginea had less effect on P. caerulea whereas the reduced (Ocan˜a, 1997). Additionally, when comparing influence of P. caerulea on P. ferruginea was striking the chlorophyll concentration associated with P. caeru- (see differences in mortality, length, weight and ability lea and P. ferruginea at the end of the experiment, we for exploiting the food resources). The destruction of observed that P. caerulea efficiently exploited food habitat and the human pressure by collecting have been resources, since it diminished chlorophyll concentration proposed as the main causes for the endangered status even at control densities, and at quadruple densities of the species (Laborel-Deguen and Laborel, 1991a; reduced the food supply below half of the original Ramos, 1998; Guerra-Garcı´a et al., 2004); in addition, amount. By contrast, chlorophyll increased dramatically the presence of some type of asymmetrical competition at control densities on P. ferruginea, whereas at quadru- would produce a weak competition ability and could be ple density, the decrease of food resources was lower a synergic factor. This possible asymmetrical interac- than for control treatment of P. caerulea, although the tion could be the consequence of their different radular biomass of P. ferruginea was greater (81.52 g/plot vs. morphology among other aspects. Although Fischer- 46.25 g/plot at the beginning of the experiment). The Piette (1935) considered the radula of P. ferruginea differences in the radula of each species, as discussed very similar to P. caerulea, Grandfils (1982) indicated above, could be the cause of the differential ability to that, whilst the number of teeth are identical, their exploit trophic resources. arrangement and morphology under the electron micro- scope are quite different. Similarly, P. caerulea is quite 4.2. Conservational implications a mobile species (personal observation) when compared with P. ferruginea, which appears relatively site specif- Enclosures (cages) modify microenvironmental con- ic (Templado, 2001; unpublished data), and the proba- ditions, as observed by Underwood (1985), reducing bility of individuals overlapping their feeding areas desiccation effects. In this way, significant differences with limpets could lead to increased competition with in physical conditions were detected inside the experi- P. ferruginea and itself. If the effects of interspecific mental plots against open surfaces that could have led competition are stronger on a species than the effects of to the increased survival observed in fenced treatments, intraspecific competition, this may lead to exclusion, together with the absence of predation and the reduction but if intraspecific competition within the superior of wave surf action. Furthermore, at quadruple densities competitor is stronger than competition between spe- of P. ferruginea (intraspecific interactions), the species cies, coexistence can occur (Boaventura et al., 2002). continued growing in both size and weight. Laborel- Finally, if intraspecific competition cannot rise beyond Deguen and Laborel (1993) proposed small, regularly certain levels without self-regulation occurring, then it spaced concentration of breeders for repopulation pro- may be impossible to exclude other species (Branch, grams as a conservation measure for P ferruginea, 1975a). P. caerulea does appear to be a species with whereas Templado (2001) noted that reintroduction of high intraspecific competition and probably with self- individuals in the Natural Park of bCabo de GataQ (SE regulation depending of density in its populations. This of Spain) would be of great interest. Additionally, scenario would allow the coexistence of both species. several engineering building may be a threat for the Regarding food supply, an inverse relationship be- species in those areas of well established populations, tween chlorophyll levels and density of limpets in the as occur in Ceuta’s harbour enlargement, where a trans- different treatments has been observed (e.g. Underwood, fer program has been implemented to avoid the death of 1984; Lasiak and White, 1993). Nevertheless, working many individuals. However, translocation of indivi- with Patella depressa and Patella vulgata, Boaventura duals has been proved to cause great mortality in a F. Espinosa et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 482–492 491 previous study conducted in the National Park of Port Dayton, P.K., 1971. Competition, disturbance and community orga- Cros in France (Laborel-Deguen and Laborel, 1991b), nization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr. 41, 351–389. where almost 50% (of 188 specimens moved) died in Fa, D., 1998. The influence of pattern and scale on the rocky-shore the first 12 h. Our study suggests that experimental macrobenthic communities through the Strait of Gibraltar. Unpub- fences used with at least eight limpets per fence or lished PhD thesis. University of Southampton, UK. more, taking into account the low intraspecific compe- Fischer-Piette, E., 1935. Syste´matique et Bioge´ographie. Les tition detected in the species, could be a useful tool for patelles d’Europe et d’Afrique du Nord. J. Conchyliol. 69 (33), 5–66. repopulating areas diminishing the mortality, together Fletcher, W.J., Creese, R.G., 1985. Competitive interactions between with defaunation in the areas of fences, to avoid the co-occurring herbivorous gastropods. Mar. Biol. 86 (2), 183–191. interspecific competition that has been revealed very Frank, P.W., 1965. The biodemography of an intertidal snail popula- important for P. ferruginea. Further studies, dealing tion. Ecology 46, 831–844. with the ecological requirements of this endangered Grandfils, R., 1982. Contribucio´n al conocimiento de Patella ferru- ginea (Gmelin, 1789). Iberus 2, 57–69. limpet need to be conducted in order to develop ade- Guerra-Garcı´a, J.M., Corzo, J., Espinosa, F., Garcı´a-Go´mez, J.C., quate strategies to conserved the species. 2004. Assessing habitat use of the endangered marine mollusc Patella ferruginea (Gastropoda, Patellidae) in northern Africa: Acknowledgements preliminary results and implications for conservation. Biol. Con- serv. 116, 319–326. Haven, S.B., 1973. Competition for food between the intertidal Special thanks to our colleagues of the Marine Bi- gastropod Acmaea scabra and Acmea digitalis. Ecology 54, ology Laboratory for their kind help with the fieldwork: 143–151. Francisco Ruiz, Roi Gonza´lez, Manuel Maestre and Iwasaki, K., 1993. The role of individual variability in limpet resting Angeles Becerra as well as to Laura Toma´s. Our grat- site fidelity and competitive ability in the organization of a local itude to staff of Parque del Mediterra´neo from Ceuta rocky intertidal community. Physiol. Ecol., Jpn. 30, 31–70. Laborel-Deguen, F., Laborel, J., 1991a. Statut de Patella ferruginea for their collaboration. The present work was funded by Gmelin en Mediterrane´e. In: Boudouresque, C.F., Avon, M., the Autoridad Portuaria de Ceuta and a PhD grant FPU Gravez, V. (Eds.), Les spe`ces marines a` prote´ger en Me´diterrane´e. AP-3556-2001 (to F. Espinosa) from the Ministry of GIS Posidonie Publishers, Marseille, pp. 91–103. 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