Morphologie,Entwicklung und Ökologie digener Trematoden-Larven der StrandschneckeLittorina littorea

More than 6000 individuals of the snailLittorina littorea L., from 6 different localities on the coast of the German Bay (North Sea), were examined for larval trematodes by crushing their shells, an additional 6000 by isolation in small quantities of sea water. Six species of larval trematodes were found inL. littorea and described: Notocotylid larva —Cercaria lebouri Stunkard, 1932; Cercaria ofHimasthla elongata (Mehlis, 1831); Cercaria ofPodocotyle atomon (Rudolphi, 1802); Cercaria ofRenicola roscovita (Stunkard, 1932) n. comb.; Metacercaria ofMicrophallus pygmaeus (Levinsen, 1881); Cercaria ofCryptocotyle lingua (Creplin, 1825). Considering the large number of investigated snails, the trematode fauna ofL. littorea in this area is assumed to be completely known. The life cycles ofHimasthla elongata andRenicola roscovita are described. Larvae of the different trematode species show differential preferences for distinct size groups of snail hosts. Juvenile snails are not infected. No correlation exists between infection rates and sex of the hosts. Quantitative aspects of multiple infections are calculated and discussed. The incidence of larval trematodes in the investigated localities differs. Information is presented on seasonal variations of infestations and their possible causes.     

Anthropogenic influences on the infestation of intertidal gastropods by seabird trematode larvae on the southern Barents Sea coast

In this study we examined how the variation in the distribution of six species of seabird trematodes was influenced by human activities along the subarctic Barents Sea coast of northern Norway. This was done by comparing the prevalence of the parasites in two species of intermediate host (Littorinasaxatilis and Littorina obtusata) on seashores near fishing industry complexes, fish farms and at control sites. In L. saxatilis there were higher prevalences at sites influenced by human activities for three out of five trematode species (Microphallus piriformes,  M. similis, Cryptocotyle lingua) which have gulls (Larus spp.) as their predominant final hosts, while in L. obtusata, only  M. similis was more common at sites with human activity. For  M. pygmaeus, a trematode which has the common eider (Somateria mollissima) as its most predominant final host, the prevalence in L.␣saxatilis tended to be higher at sites with fishing industry, but differences were not significant. No such tendency was found in L. obtusata for this trematode. The overall prevalence in L. obtusata was lower than in L.␣saxatilis. This indicates that the vulnerability to trematode infection differs between the two snail species depending on the variation in the distribution patterns in the intertidal zone. Gulls tend to concentrate in areas near fishing industry and fish farms to feed on fish offal, which leads to an increase in the transmission between hosts, and to a higher level of parasite infection, locally. Received: 4 May 1998 / Accepted: 18 October 1998     

Geographic variation in the growth rates of Littorina littorea and L. saxatilis

The two intertidal grazers Littorina littorea and L. saxatilis occupy extensively overlapping distributions on both sides of the Atlantic. Morphological, electrophoretic and physiological evidence suggests that the direct developer L. saxatilis is more geographically differentiated than the planktonic developer L. littorea. This hypothesis was tested by collecting both species in 1980 and 1981 from three geographically separated beaches in Massachusetts, USA, marking them, and releasing them in two of the sites. Individuals from all three L. littorea populations, grown at a common site, tended to grow at similar rates, while L. saxatilis exhibited consistent population differences in individual growth. This study supports the view that L. saxatilis achieves its broad geographic distribution via locally adapted ecotypes, while L. littorea achieves its distribution by individual physiological plasticity.     

The introduction of Littorina littorea to British Columbia, Canada: potential impacts and the importance of biotic resistance by native predators

Although the establishment and spread of non-indigenous species depends upon survival in the face of novel environmental conditions and novel biological interactions, relatively little attention has been focused on the specific role of native predators in limiting invasion success. The European common periwinkle, Littorina littorea, was recently introduced to the Pacific coast of Canada and provides a case study of an introduction into an area with an important predator guild (sea stars) that is functionally minor in the invader’s native habitat. Here, we assess the likelihood of establishment, spread, and negative ecological impact of this introduced gastropod, with an emphasis on the role of native sea stars as agents of biotic resistance. Size frequency distributions and local market availability suggest that L. littorea was most likely introduced via the live seafood trade. Non-native hitchhikers (e.g., the trematode Cryptocotyle lingua) were found on/in both market and field specimens. Laboratory studies and field observations confirmed that L. littorea can survive seasonal low salinity in Vancouver, British Columbia. Periwinkles also readily consumed native Ulva, suggesting that periwinkles could impact native communities via herbivory or resource competition. Unlike native gastropods, however, L. littorea lacked behavioural avoidance responses to Northeast Pacific predatory sea stars (Pisaster ochraceus and Pycnopodia helianthoides), and sea star predation rates on L. littorea were much higher than predation rates on native turban snails (Chlorostoma funebralis) in common garden experiments. We therefore expect periwinkle establishment in British Columbia to be limited to areas with low predator density, as is seen in its field distribution to date. We caution that this conclusion may understate the importance of the L. littorea introduction if it also serves as a vector for additional non-indigenous species such as C. lingua.     

Biochemical composition and energy reserves in the larvae and adults of the four british periwinkles Littorina littorea,L. littoralis,L. saxatilis and L. neritoides

The biochemical composition of the adult body tissue is similar in Littorina littorea, L. littoralis, L. saxatilis and L. neritoides. In the newly crawling metamorphosed young of L. littoralis and L. saxatilis, the biochemical composition is similar to that of the mature adults. The newly released planktonic veliger larvae of L. littorea and L. neritoides, which represent and earlier stage of development than the newly crawling young, have a neutral lipid level (mean, 16.5% of ash-free dry flesh weight) approximately three times the level (5.4%) in the newly crawling young of L. littoralis and L. saxatilis. Otherwise the biochemical composition of free-swimming larvae is similar to that of newly crawling young and adults. Neutral lipid is apparently utilised by L. littoralis and L. saxatilis larvae during larval development and metamorphosis. It is suggested that neutral lipid is the major energy reserve of Littorina veliger larvae whereas in the adults, as exemplified by L. littorea, both lipid and carbohydrate are important as energy reserves.     

Reproductive biology of three species of midwater fishes associated with the continental slope of eastern Tasmania,Australia

The reproductive biology of Lampanyctodes hectoris (Günther, 1876), Maurolicus muelleri (Gmelin, 1789) and Diaphus danae Tåning, 1932, from continental-slope waters of eastern Tasmania, was examined between April 1984 and June 1985. L. hectoris spawned in winter and M. muelleri spawned from late winter to early summer. Apart from one ripe male, no reproductive activity was detected in D. danae; this species may be an expatriate in these waters. Fecundity was positively correlated with standard length in L. hectoris, but not in M. muelleri. The ratio of females to males increased with length in all three species. The spermatozoa of L. hectoris and D. danae are atypical of vertebrates and have no tail.     

Combining gut fluorescence technique and spatial analysis to determine <Emphasis Type="Italic">Littorina littorea</Emphasis> grazing dynamics in nutrient-enriched and nutrient-unenriched littoral mesocosms

Spatiotemporal distribution patterns in relation to feeding behavior of herbivorous gastropods have been studied extensively, but still knowledge about small-scale patterns is limited in relation to eutrophication. This experimental study aimed to describe the small-scale distribution of Littorina littorea in nutrient-enriched and nutrient-unenriched mesocosms in a merely atidal region and relate the distribution to food abundance and possible competing organisms, while checking simultaneously for feeding activities. The latter part was accomplished through the “gut fluorescence technique” GFT (which, to our knowledge, has not previously been used for benthic grazers) to estimate per capita grazing rates and the former part through monitoring of spatial heterogeneity of L. littorea and co-variation with sessile organisms (using semivariograms and cross-semivariograms, respectively). After 5 months of nutrient addition, the abundance and biomass of L. littorea had increased in enriched systems, which also had significantly higher total biomass of green algae. Gut pigment content was higher in L. littorea from enriched mesocosms, and gut depletion rate was higher in L. littorea from unenriched mesocosms. Spatial analysis showed that L. littorea exhibited generally random patterns (suggesting feeding activities) but sometimes (often in the morning) spatial patchiness (clumped distribution) in both enriched and unenriched conditions. There was mainly positive co-variation between L. littorea and biofilm, while different nutrient conditions exhibited contrasting co-variation between L. littorea and barnacles (positive co-variation in enriched and negative co-variation in unenriched mesocosms). The study offered insights into how feeding behavior and spatial distribution of a species may interact with community components differently under different nutrient regimes. The applied methodology can be useful for purposes of faster examination of grazing effects among different regions and also to compare grazing intensities and interactions between grazers and the benthic communities in disturbed (including pollution and nutrient enrichment) and non-disturbed systems, as well as in up-welling versus non-upwelling areas.     

Seasonal variations in distribution and population structure of Microcalanus pygmaeus and Ctenocalanus citer (Copepoda: Calanoida) in the eastern Weddell Sea,Antarctica

The abundance, vertical distribution and population structure of two important small calanoid copepod species, Microcalanus pygmaeus (G. O. Sars) and Ctenocalanus citer Heron and Bowman, were studied in the eastern Weddell Sea in summer (January/February 1985), in late winter/early spring (October/November 1986) and in autumn (April/May 1992). The population of Microcalanus pygmaeus consisted mainly of copepodite stages CII and CIII in late winter/early spring and were concentrated between 500 and 200 m depth. In summer, stage CIV was the modal stage and the bulk of the population had ascended above 300 m. In autumn the population structure was bimodal with CI and CV dominating. Most of the population was concentrated between 300 and 200 m. In all investigation periods M. pygmaeus had their maximal concentrations in the thermo-pycnocline. The developmental stages CIII to CV of Ctenocalanus citer formed the bulk of the population in late winter/early spring. In October all developmental stages had their main distribution between 500 and 200 m, except females, which were concentrated in the upper 50 m. In November most of the population occurred between 200 and 50 m. The summer population was concentrated in the upper 50 m, and numbers increased dramatically as the new cohort hatched. Copepodite stages CII and CIII dominated the population at the end of January, while CIV dominated 2 wk later. In autumn, CV was the modal stage. The majority of the population was concentrated in the upper 100 m, but there was an increase in abundance below 300 m compared to summer. Age structure changed with depth with a younger surface population and an older one in deeper water layers. The seasonal change in number of M. pygmaeus is much smaller than that of C. citer; the summer:winter:autumn ratio of the former being about one, whereas the winter:summer/autumn of the latter was about nine. Early copepodite stages and adults of M. pygmaeus occurred throughout all investigation periods. The large proportion of early copepodite stages in April and in mid-October suggests autumn and early to midwinter breeding. Apparently, M. pygmaeus may reproduce and grow year-round or perhaps has a 2-yr life-cycle. In contrast, the dramatic increase in abundance of early copepodite stages of C. citer in summer suggests springtime reproduction.     

Predator-induced alarm responses in the common periwinkle, Littorina littorea: dependence on season, light conditions, and chemical labelling of predators

Chemically mediated alarm reactions of the common periwinkle, Littorina littorea (L.), were studied in laboratory experiments during two consecutive summers, and one intermediate autumn season. Responses to chemical stimuli were detected as crawl-out responses, i.e. movements of snails out of the water. Snails were exposed to extracts of injured conspecifics, extracts of the mussel Modiolus modiolus (L.), and water conditioned by the predatory crab Carcinus maenas (L.), which had been maintained on different diets. In experiments carried out during the summer, a significantly larger number of snails moved out of the water when exposed to chemical stimuli from injured conspecifics, compared to chemical stimuli from injured mussels or filtered seawater. These results suggest that chemical alarm substances are present in L. littorea. Water conditioned by crabs that had been fed L. littorea released significantly more crawl-out responses compared to water conditioned by crabs that had been kept on a fish diet. When tested in autumn, no significant differences were found in responses to the above-mentioned water samples. Crawl-out responses under different light regimes were also investigated. All series of experiments carried out in the dark evoked a higher number of responses compared to series that took place in light. These findings may indicate an adaptation of snails to night-active predators. In total, the current results suggest that a L. littorea diet may chemically “label” the predator crab with snail alarm substances, and that predator-induced responses of L. littorea are actually responses to conspecific alarm substances released from crabs that have been maintained on a L. littorea diet. The response to the alarm signal, however, appears to be dependent on season and light conditions; some ecological implications of these findings are also discussed. Received: 8 January 1999 / Accepted: 29 March 1999     

Genetic differentiation in Littorina saxatilis (Gastropoda)

Littorina saxatilis, an ovoviviparous gastropod, displays considerable morphological variability, perhaps due to limited dispersal abilities. Gene and genotype frequencies of 2 polymorphic enzymatic loci were determined electrophoretically for 7 populations of L. saxatilis, to estimate degree of population differentiation. Results show that significant population differentiation may occur over distances of as little as 2 km, while widely separated populations may be nearly identical. An index of probability of genotypic identity calculated for populations of L. saxatilis shows variable and heterogeneous values. Comparison of this index for L. saxatilis with an index for 12 populations of Nassarius obsoletus —which possesses strong dispersal abilities due to long-term veliger larva and high, homogeneous indices of probability of genotypic identity between populations — indicates a strong correlation between population differentiation and dispersal ability of the organism. Possible factors influencing population differentiation in L. saxatilis are discussed.     

Evaluation of the significance of metal-binding proteins in the gastropod Littorina littorea

Measurements of metals in Littorina littorea from clean and contaminated sites in Great Britain confirmed that body concentrations of Ag, Cd and Hg vary according to environmental contamination, while the essential elements Cu and Zn are regulated. Investigation of the cytosolic distribution of metals in L. littorea, using Sephadex G-75 gel-permeation chromatography, revealed important distinctions in the partitioning of elements. In contrast to Ag and Hg, which were mainly associated with high molecular weight ligands, Cd was bound predominantly to an intermediate molecular weight, soluble protein (CdBP-I, apparent mol. wt=20 000). However, although the main function of CdBP-I, both in clean as well as contaminated individuals, was sequestration of Cd, significant quantities of other non-essential metals (Ag, Hg) were similarly bound. Laboratory experiments confirmed the role of CdBP-I in complexing cadmium, and also revealed the induction of a second cadmium-binding protein (CdBP-II) in response to high cadmium levels. The apparent molecular weight (10 000), absorbance characteristics and high (inducible)-SH content of CdBP-II suggest similarities with metallothionein. A dose-related increase in the-SH content of very low molecular weight (>3 000) fractions was also observed in cadmium-exposed L. littorea, although no cadmium was associated with these ligands. A detoxifying role is tentatively proposed for the metal-binding proteins CdBP-I and II in L. littorea. However, some spillover of cadmium to the high molecular weight protein pool was observed in individuals exposed to cadmium in the field and laboratory. The use of L. littorea in biochemical assays of environmental contamination is discussed.     

Conflict of interest between a nematode and a trematode in an amphipod host: test of the "sabotage" hypothesis

Microphallus papillorobustus is a manipulative trematode that induces strong behavioural alterations in the gamaridean amphipod Gammarus insensibilis, making the amphipod more vulnerable to predation by aquatic birds (definitive hosts). Conversely, the sympatric nematode Gammarinema gammari uses Gammarus insensibilis as a habitat and a source of nutrition. We investigated the conflict of interest between these two parasite species by studying the consequences of mixed infection on amphipod behaviour associated with the trematode. In the field, some amphipods infected by the trematode did not display the altered behaviour. These normal amphipods also had more nematodes, suggesting that the nematode overpowered the manipulation of the trematode, a strategy that would prolong the nematode's life. We hypothesize that sabotage of the trematode by the nematode would be an adaptive strategy for the nematode consistent with recent speculation about co-operation and conflict in manipulative parasites. A behavioural test conducted in the laboratory from naturally infected amphipods yielded the same result. However, exposing amphipods to nematodes did not negate or decrease the manipulation exerted by the trematode. Similarly, experimental elimination of nematodes from amphipods did not permit trematodes to manipulate behaviour. These experimental data do not support the hypothesis that the negative association between nematodes and manipulation by the trematode is a result of the "sabotage" hypothesis.     

Latitudinal differences in host-specificity of marine Monogenea and digenea

Data from 15 surveys of marine trematodes (average of 91 trematode species and more than 80 fish species per survey) and from 12 surveys of marine Monogenea (average of 52 Monogenea species and more than 49 fish species per survey) show that the degree of host specificity of marine digenetic trematodes increases from cold to warm seas; Monogenea do not show such a trend, and the trend is probably reversed in the Pacific Ocean. The difference between the two groups is explained in terms of r ^- and k ^- strategy. Monogenea tend to follow a k ^- strategy (great complexity of adult, few offspring), which results in a high degree of host- and sitespecificity to facilitate mating in low-density populations. Only one or a few related host species can be infected, and as more related host species are present in the warm Pacific, host-specificity there is reduced. Digenea tend to follow an r^- strategy (simple strucure of adult, many offspring), part of which is to infect many ecologically suitable hosts. Host-specificity in cold-temperate seas is reduced because of the less patchy and ecologically less restricted distribution of hosts.     

Shell selection in the hermit crab Pagurus bernhardus

Three shell variables were deemed to be important in the selection of a shell by the hermit crab Pagurus bernhardus (L.). These were the weight, volume and aperture width of a shell. Each of these variables were used in multiple regressions against crab weight for 25 Littorina littorea and 25 Thais lapillus shells chosen when both shell species were together in a tank, and for a further 25 L. littorea and 25 T. lapillus when the two shell species were separate. Principal component analysis was performed on the four groups of 25 shells selected, and multiple-regression equations were calculated using the principal components as the new variables. It was found that crabs chose a shell of suitable general dimensions rather than solely on the basis of one shell variable. The advantages of using statistical techniques developed in this paper over previous approaches to shell selection are discussed.     

Non-host organisms affect transmission processes in two common trematode parasites of rocky shores

The transmission of free-living trematode stages is mediated by various environmental factors, of which the presence of ambient organisms within the host space is a potential major determinant. In two laboratory mesocosm experiments, we investigated the influence of four intertidal rocky shore species on transmission success of cercariae of the digenean trematodes Echinostephilla patellae (encysting in the tissue of blue mussels Mytilus edulis) and Parorchis acanthus (encysting on mussel shells). Encystment success of both parasite species was significantly lower in the presence of test organisms when compared to controls. Observations revealed that barnacles Austrominius modestus actively filtered cercariae, whereas the larvae were obstructed by the seaweeds Corallina officinalis and Fucus serratus. Anemones Actinia equina both physically disturbed and consumed cercariae. In a further laboratory experiment, grazing gastropods (Littorina littorea, Patella vulgata, and Gibbula umbilicalis) were found to significantly reduce the numbers of P. acanthus metacercariae in artificially prepared dishes by ingestion of cysts. Our results suggest that non-host organisms may play a key role in regulating the transmission of free-living trematode stages in rocky shore ecosystems, which is especially important with regard to the relative diversity and density of species in these habitats. The findings also emphasize the need to include parasites into marine food webs, since cercariae seem to be consumed by certain organisms to a considerable extent and could possibly represent an important energy source.     

Effects of Lunatia heros predation on the population dynamics of Mya arenaria and Macoma balthica in Maine,USA

The interaction between the naticid snail predator Lunatia heros and 2 iteroparous, infaunal, intertidal bivalves was investigated in Lubec, Maine, USA. The Mya arenaria population consists primarily of young, small individuals. M. arenaria survivorship is low when young (3.5% yr^-1 for the first 5 yr), then increases. M. arenaria can attain a length of 60 mm, but it is susceptible to L. heros attack only until it is 30 mm long. It delays reproduction until it is 20 mm long (3.8 yr) and diverts its resources instead into rapid early growth (4.9 mm yr^-1 for the first 5 yr). The Macoma balthica population has a larger proportion of older individuals than does that of M. arenaria. Survivorship is higher for M. balthica than for M. arenaria (76.3% yr^-1 for the first 5 yr). Unlike M. arenaria, M. balthica attains a final length of only 25 mm and all sizes are susceptible to L. heros attack. M. balthica grows slowly (2.7 mm yr^-1 for the first 5 yr) and diverts its resources into earlier reproduction at a length of 10 mm (2.9 yr). These contrasting life-history patterns and the possible relationship between bivalve resource allocation and refuges from predation are discussed.     

Relating bird host distribution and spatial heterogeneity in trematode infections in an intertidal snail—from small to large scale

Shorebird abundance and spatial distribution of larval trematodes in the New Zealand mudsnail, Zeacumantus subcarinatus, were investigated in soft-sediment intertidal bays within Otago Harbour, South Island, New Zealand. In a small-scale study, recruitment of trematodes to caged sentinel snails and the prevalence of infection in free-living snails were examined across a grid of fifteen 50×25 m plots arranged in a representative area of an intertidal bay, in relation to within-plot shorebird abundance (definitive hosts) and tidal height. In a large-scale study, natural spatial variation of larval trematodes in Z. subcarinatus was examined across 12 bays in relation to local abundance of shorebirds. Our results revealed that trematode prevalence in snails was positively correlated with bird abundance across bays (R ²=0.503, P=0.006). In contrast, despite a difference in bird abundance between tidal heights, there was no evidence that trematode prevalence reflected the spatial distribution of birds in the small-scale study, suggesting that factors related to differences in submersion time may override the differential input of trematode eggs from birds.     

Parasites of the chaetognath Sagitta setosa in the western English Channel

The temporal occurrence of parasites in Sagitta setosa J. Müller, caught one to three times a month during 1982 and 1983 off Plymouth, England, was investigated. S. setosa was infected by eight parasitic species: one nematode, five trematodes, one cestode and, possibly, one protozoon. Infection by a single parasite, normally found in the body coelom, was the rule. The nematode Hysterothylacium aduncum, as III-stage larva, was by far the most common parasite (56% of all parasites found), followed by the metacercariae of three non-encysted trematodes: Derogenes varicus, a didymozoid species and a Lecithochirium species. Two trematode species new to Chaetognatha were found. The percentage of infected S. setosa specimens ranged from 0 to 7%. Absence or low numbers of parasites from June to November were correlated to the disappearance of large S. setosa and the appearance of a new S. setosa generation. Trematodes may show great annual and seasonal differences in occurrence in S. setosa. No injuries due to parasites were seen. The reproduction of the S. setosa populations off Plymouth did not seem to be affected by parasite infections during 1982–1983.     

Diel and lunar patterns of reproduction in the Caribbean and Pacific sergeant major damselfishes Abudefduf saxatilis and A. troschelii

Diel and lunar reproductive patterns of the Caribbean and Pacific sergeant major damselfishes Abudefduf saxatilis and A. troschelii respectively, were studied i the San Blas and Northern Perls Islands of Panama in 1981 and 1982. These are sister-species that have diverged since the uplift of the isthmus of Panama. Caribbean A. saxatilis females typically complete spawning in the nests of males earlier in the morning than do Pacific A. troschelii females. Spawning is rarely observed during the afternoon. Hatching occurs four or five days after spawning in the Caribbean species, and after four days in the Pacific species. In both, fry hatch during the hour following sunset. There also are differences in lunar patterns of spawning between the two species. The Caribbean A. saxatilis spawns throughout the month, exhibiting no lunar periodicity. In the Pacific A. troschelii spawns within nine days on either side of new moon. During the wet season, reproductive activity at a site spans three or four days, but is extended to eight or more days during dry season upwelling in the Bay of Panama. Thus, reproductive synchrony is much greater within than between colonies of the Pacific sergeant major, particularly in the wet season. Reproductive synchrony in the Pacific sergeant major might be beneficial because fry hatching at dusk encounter favorable tides for transport away from reef-based predators around new moon, or because reproductive synchrony reduces the risk of predation on unhatched embryos in nests guarded by males. Tidal amplitude and the rate of predation on embryos in nests are greater in the Pacific.     

Conservation genetics of <Emphasis Type="Italic">Lumnitzera littorea</Emphasis> (Combretaceae), an endangered mangrove,from the Indo-West Pacific

Mangrove forests, with their ecological significance and economic benefits, are vital inter-tidal wetland ecosystems. Lumnitzera littorea (Combreataceae) is a non-viviparous mangrove distributed in tropical Asia and North Australia. Due to natural and human impacts, populations of this species have been isolated, fragmented, and highly disturbed. In China, L. littorea is an endangered species, restricted to small regions of Hainan Island. The genetic composition of five populations of this species from the Indo-West Pacific (South China, Malay Peninsula, Sri Lanka, North Australia) was assessed using inter simple sequence repeat (ISSR) makers. At the species level, expected mean heterozygosity (He) was 0.240 with 75.6% of loci polymorphic (P). However, genetic variation was much lower at the population level (P = 37.1%, He = 0.118). A high coefficient of gene differentiation (Gst = 0.515) and low level of gene flow (Nm = 0.470) indicated significant genetic differentiation among populations. AMOVA also indicated that more than half the total variation (58.4%) was partitioned among populations. The high degree of differentiation observed among populations emphasizes the need for appropriate conservation measures that incorporate additional populations into protected areas, and achieve the restoration of separate, degraded populations.