Symbiosis regulation in a facultatively symbiotic temperate coral: zooxanthellae division and expulsion

Zooxanthellae mitotic index (MI) and expulsion rates were measured in the facultatively symbiotic scleractinian Astrangia poculata during winter and summer off the southern New England coast, USA. While MI was significantly higher in summer than in winter, mean expulsion rates were comparable between seasons. Corals therefore appear to allow increases in symbiont density when symbiosis is advantageous during the warm season, followed by a net reduction during the cold season when zooxanthellae may draw resources from the coral. Given previous reports that photosynthesis in A. poculata symbionts does not occur below approximately 6°C, considerable zooxanthellae division at 3°C and in darkness suggests that zooxanthellae are heterotrophic at low seasonal temperatures. Finally, examination of expulsion as a function of zooxanthellae density revealed that corals with very low zooxanthellae densities export a significantly greater proportion of their symbionts, apparently allowing them to persist in a stable azooxanthellate state.     

Bleaching in coral reef anthozoans: effects of irradiance,ultraviolet radiation,and temperature on the activities of protective enzymes against active oxygen

Recent widespread bleaching of coral reef anthozoans has been observed on the Great Barrier Reef, the Pacific coast of Panama, and in the Caribbean Sea. Bleaching events have been correlated with anomalously high sea surface temperatures which are presumed to cause the expulsion of zooxanthellae from their hosts. Our experimental results show that increases in temperature significantly reduce the total number of zooxanthellae per polyp. At the same time temperature, irradiance (photosynthetically active radiation=PAR), and ultraviolet radiation (UV) independently increase the activities of the enzymes superoxide dismutase, catalase, and ascorbate peroxidase within the zooxanthellae of the zoanthid Palythoa caribaeorum. Enzyme activities within the host are only suggestive of similar changes. These enzymes are responsible for detoxifying active forms of oxygen, and their elevated activities indirectly indicate an increase in the production of active oxygen species by increases in these environmental factors. Historically, bleaching has been attributed to changes in temperature, salinity, and UV. Increases in temperature or highly energetic UV radiation can increase the flux of active forms of oxygen, particularly at the elevated oxygen concentrations that prevail in the tissues during photosynthesis, with oxygen toxicity potentially mediating the bleaching event. Additionally, the concentration of UV absorbing compounds within the symbiosis is inversely related to temperature, potentially increasing exposure of the host and zooxanthellae to the direct effects of UV.     

Is photoinhibition of zooxanthellae photosynthesis the primary cause of thermal bleaching in corals?

The bleaching of corals in response to increases in temperature has resulted in significant coral reef degradation in many tropical marine ecosystems. This bleaching has frequently been attributed to photoinhibition of photosynthetic electron transport and the consequent photodamage to photosystem II (PSII) and the production of damaging reactive oxygen species (ROS) in the zooxanthellae (Symbiodinium spp.). However, these events may be because of perturbations of other processes occurring within the zooxanthellae or the host cells, and consequently constitute only secondary responses to temperature increase. The processes involved with the onset of photoinhibition of electron transport, photodamage to PSII and pigment bleaching in coral zooxanthellae are reviewed. Consideration is given to how increases in temperature might lead to perturbations of metabolic processes in the zooxanthellae and/or their host cells, which could trigger events leading to bleaching. It is concluded that production of ROS by the thylakoid photosynthetic apparatus in the zooxanthellae plays a major role in the onset of bleaching resulting from photoinhibition of photosynthesis, although it is not clear which particular ROS are involved. It is suggested that hydrogen peroxide generated in the zooxanthellae may have a signalling role in triggering the mechanisms that result in expulsion of zooxanthellae from corals.     

The influence of irradiance on the severity of thermal bleaching in sea anemones that host anemonefish

Entacmaea quadricolor is a geographically widespread species of sea anemone that forms a three-way symbiosis with anemonefish and Symbiodinium. This species dominates the reef substrata at North Solitary Island, Australia, which is located in a region identified as a climate change hot spot. Their geographic location places these anemones under significant threat from rising ocean temperatures, although their upper thermal limit and risk of bleaching are unknown. To address this knowledge gap, anemones were exposed to one of four temperatures (23, 25, 27, or 29°C) and one of two irradiance treatments (high or low light) over 6 days. At moderate temperatures (27°C, 1°C above summer average), anemone bleaching was characterised by symbiont expulsion, while extreme temperatures (29°C) resulted in an additional loss of photosynthetic pigments from within symbionts, and in some cases, host mortality. Irradiance influenced the susceptibility to thermal stress with high light promoting the bleaching response, along with significant reductions in the effective quantum yield of anemone symbionts. The long-term loss of photosystem II photochemical efficiency within in hospite symbionts was observed during exposure to temperatures exceeding the summer average, indicating photosynthetic damage. The resident Symbiodinium, identified as clade C using 28S rRNA gene sequences, therefore represents the partner within the symbiosis that is likely to be most vulnerable to rising seawater temperatures. Results suggest that E. quadricolor is living within approximately 1°C of the upper thermal maximum at the Solitary Islands, and given the predictions for rising seawater temperature on Australia’s east coast, the thermal threshold at which bleaching will occur is expected to be reached and exceeded more frequently in the future.     

The role of symbiotic dinoflagellates in the temperature-induced bleaching response of the subtropical sea anemone Aiptasia pallida

Coral bleaching involves the loss of symbiotic dinoflagellates (zooxanthellae) from reef corals and other cnidarians and may be a stress response of the host, algae or both. To determine the role of zooxanthellae in the bleaching process, aposymbiotic sea anemones from Bermuda (Aiptasia pallida) were infected with symbionts from other sea anemones (Aiptasia pallida from Florida, Bartholomea annulata and Condylactis gigantea). The expulsion of algae was measured during 24-h incubations at 25, 32 and 34 degrees C. Photosynthetic rates of freshly isolated zooxanthellae were also measured at these temperatures. The C. gigantea (Cg) symbionts were expelled in higher numbers than the other algae at 32 degrees C. Photosynthesis by the Cg algae was completely inhibited at this temperature, in contrast to the other symbionts. At 34 degrees all of the symbionts had increased expulsion rates, and at this temperature only the symbionts from Florida A. pallida exhibited any photosynthesis. These results provide the first evidence that the differential release of symbionts from the same host species is related to decreased photosynthesis at elevated temperatures, and support other findings suggesting that zooxanthellae are directly affected by elevated temperatures during bleaching events.     

Neutralization of radical toxicity by temperature-dependent modulation of extracellular SOD activity in coral bleaching pathogen Vibrio shiloi and its role as a virulence factor

Vibrio shiloi is the first and well-documented bacterium which causes coral bleaching, particularly, during summer, when seawater temperature is between 26 and 31°C. Coral bleaching is the disruption of the symbiotic association between coral hosts and their photosynthetic microalgae zooxanthellae. This is either due to lowered resistance in corals to infection or increased virulence of the bacterium at the higher sea surface temperature. The concentration of the oxygen and resulting oxygen radicals produced by the zooxanthellae during photosynthesis are highly toxic to bacteria, which also assist corals in resisting the infection. Hence, in this study we examined the effect of different temperatures on the activity of a novel extracellular SOD in V. shiloi. We also partially characterized the SOD and clearly confirmed that the extracellular SOD produced by V. shiloi is Mn–SOD type, as it was not inhibited by H₂O₂ or KCN. Performing chemical susceptibility killing assay, we confirmed that extracellular SOD may act as first line of defense for the bacteria against the reactive oxygen species. Since, increased activity of novel Mn–SOD at higher temperature, leads to the neutralization of radical toxicity and facilitates the survival of V. shiloi. Hence, the extracellular Mn–SOD may be considered as a virulence factor.     

BROAD THERMAL TOLERANCE OF THE SYMBIOTIC DINOFLAGELLATE SYMBIODINIUM MUSCATINEI (DINOPHYTA) IN THE SEA ANEMONE ANTHOPLEURA ELEGANTISSIMA (CNIDARIA) FROM NORTHERN LATITUDES1

The sea anemone Anthopleura elegantissima (Brandt) hosts two species of symbiotic dinoflagellates, known as zooxanthellae, which coexist within the host at southern latitudes only. One of these species, Symbiodinium muscatinei LaJeunesse et Trench, has a broad latitudinal distribution, occurring in intertidal anemones from Washington state to Southern California. To investigate whether high thermal tolerance contributes to the ability of S. muscatinei to inhabit anemones from northern and southern regions, the upper thermal tolerance limit for photosynthesis of symbionts in northern (48°24′ N) populations of A. elegantissima was determined by subjecting anemones to a gradual increase in temperature from 12°C to 30°C over a 10‐week period. Light‐saturated photosynthetic rates of isolated zooxanthellae were the same over the range of 12°C–24°C and declined significantly at 26°C, which is 14°C and 5°C above average summertime seawater temperatures in northern Puget Sound and Southern California, respectively. At 28°C, zooxanthellae isolated from the anemones, and those expelled by their hosts, exhibited extremely low rates of photosynthesis and highly reduced chl content. The photosynthetic rates and chl content of expelled zooxanthellae were lower than those of retained zooxanthellae. The high thermal tolerance of S. muscatinei isolated from northern populations of anemones supports the broad latitudinal distribution of this symbiont, allowing it to coexist with S. californium (#383, Banaszak et al. 1993 ) in southern populations of anemones.     

Finding of 132, 173‐cyclopheophorbide a enol as a degradation product of chlorophyll in shrunk zooxanthellae of the coral Montipora digitata

We examined the morphology and pigment composition of zooxanthellae in corals subjected to normal temperature (27°C) and thermal stress (32°C). We observed several normal and abnormal morphological types of zooxanthellar cells. Normal cells were intact and their chloroplasts were unbroken (healthy); abnormal cells were shrunken and had partially degraded or broken chloroplasts, or they were bleached and without chloroplasts. At 27°C, most healthy zooxanthellar cells were retained in the coral tissue, whereas shrunken zooxanthellae were expelled. Under thermal stress, the abundance of healthy zooxanthellae declined and the proportion of shrunken/abnormal cells increased in coral tissues. The rate of algal cell expulsion was reduced under thermal stress. Within the shrunken cells, we detected the presence of a chl‐like pigment that is not ordinarily found in healthy zooxanthellae. Analysis of the absorption spectrum, absorption maxima, and retention time (by HPLC) indicated that this pigment was 13², 17³‐cyclopheophorbide a enol (cPPB‐aE), which is frequently found in marine and lacustrine sediments, and in protozoans that graze on phytoplankton. The production of cPPB‐aE in shrunken zooxanthellae suggests that the chls have been degraded to cPPB‐aE, a compound that is not fluorescent. The lack of a fluorescence function precludes the formation of reactive oxygen species. We therefore consider the formation of cPPB‐aE in shrunken zooxanthellae to be a mechanism for avoiding oxidative stress.     

Impacts of bleaching on the soft coral Lobophytum compactum. I. Fecundity, fertilization and offspring viability

We document long-term effects of a simulated bleaching event on the reproductive output and offspring viability of the soft coral Lobophytum compactum. Corals were subjected to temperature and solar radiation treatments to produce both moderately (48–60%) and heavily (90–95%) bleached colonies. Although bleached colonies recovered their zooxanthellae within 10 to 18 weeks, impacts on reproductive output were significant for at least two annual spawning seasons. In the first year, both polyp fecundity and mean oocyte diameter were reduced and inversely correlated with the degree of bleaching, with complete failure of fertilization in the group of heavily bleached colonies. For moderately bleached soft corals, survival and growth of sexual offspring did not differ significantly from those of unbleached colonies. Although no further reductions in zooxanthellae densities in experimental soft corals were recorded throughout the subsequent second year, egg size and fecundity of the heavily bleached soft corals were still significantly reduced 20 months later. Severe bleaching clearly has long-term sub-lethal impacts, reducing overall reproductive output for at least two spawning seasons. Accepted: 1 June 2000     

Catalase characterization and implication in bleaching of a symbiotic sea anemone

Symbiotic cnidarians are marine invertebrates harboring photosynthesizing microalgae (named zooxanthellae), which produce great amounts of oxygen and free radicals upon illumination. Studying antioxidative balance is then crucial to understanding how symbiotic cnidarians cope with ROS production. In particular, it is suspected that oxidative stress triggers cnidarian bleaching, i.e., the expulsion of zooxanthellae from the animal host, responsible for symbiotic cnidarian mass mortality worldwide. This study therefore investigates catalase antioxidant enzymes and their role in bleaching of the temperate symbiotic sea anemone Anemonia viridis. Using specific separation of animal tissues (ectoderm and endoderm) from the symbionts (zooxanthellae), spectrophotometric assays and native PAGE revealed both tissue-specific and activity pattern distribution of two catalase electrophoretypes, E1 and E2. E1, expressed in all three tissues, presents high sensitivity to the catalase inhibitor aminotriazole (ATZ) and elevated temperatures. The ectodermal E1 form is responsible for 67% of total catalase activity. The E2 form, expressed only within zooxanthellae and their host endodermal cells, displays low sensitivity to ATZ and relative thermostability. We further cloned an ectodermal catalase, which shares 68% identity with mammalian monofunctional catalases. Last, 6 days of exposure of whole sea anemones to ATZ (0.5 mM) led to effective catalase inhibition and initiated symbiont expulsion. This demonstrates the crucial role of this enzyme in cnidarian bleaching, a phenomenon responsible for worldwide climate-change-induced mass mortalities, with catastrophic consequences for marine biodiversity.     

Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae

The early effects of heat stress on the photosynthesis of symbiotic dinoflagellates (zooxanthellae) within the tissues of a reef-building coral were examined using pulse-amplitude-modulated (PAM) chlorophyll fluorescence and photorespirometry. Exposure of Stylophora pistillata to 33 and 34 °C for 4 h resulted in (1) the development of strong non-photochemical quenching (qN) of the chlorophyll fluorescence signal, (2) marked decreases in photosynthetic oxygen evolution, and (3) decreases in optimal quantum yield (F_v/F_m) of photosystem II (PSII). Quantum yield decreased to a greater extent on the illuminated surfaces of coral branches than on lower (shaded) surfaces, and also when high irradiance intensities were combined with elevated temperature (33 °C as opposed to 28 °C). qN collapsed in heat-stressed samples when quenching analysis was conducted in the absence of oxygen. Collectively, these observations are interpreted as the initiation of photoprotective dissipation of excess absorbed energy as heat (qN) and O₂-dependent electron flow through the Mehler-Ascorbate-Peroxidase cycle (MAP-cycle) following the point at which the rate of light-driven electron transport exceeds the capacity of the Calvin cycle. A model for coral bleaching is proposed whereby the primary site of heat damage in S. pistillata is carboxylation within the Calvin cycle, as has been observed during heat damage in higher plants. Damage to PSII and a reduction in F_v/F_m (i.e. photoinhibition) are secondary effects following the overwhelming of photoprotective mechanisms by light. This secondary factor increases the effect of the primary variable, temperature. Potential restrictions of electron flow in heat-stressed zooxanthellae are discussed with respect to Calvin cycle enzymes and the unusual status of the dinoflagellate Rubisco. Significant features of our model are that (1) damage to PSII is not the initial step in the sequence of heat stress in zooxanthellae, and (2) light plays a key secondary role in the initiation of the bleaching phenomena.     

The effects of elevated temperature on the photosynthetic efficiency of zooxanthellae in hospite from four different species of reef coral: a novel approach

Bleaching of reef corals is a phenomenon linked to temperature stress which involves loss of the symbiotic algae of the coral, which are known as zooxanthellae, and/or loss of algal pigments. The photosynthetic efficiency of zooxanthellae within the corals Montastrea annularis, Agaricia lamarki, Agaricia agaricites and Siderastrea radians was examined by pulse-amplitude modulation fluorometry (PAM) during exposure to elevated temperatures (30–36°C). Zooxanthellae within M. annularis and A. lamarki were found to be more sensitive to elevated temperature, virtually complete disruption of photosynthesis being noted during exposure to temperatures of 32 and 34°C. The photosynthetic efficiency of zooxanthellae within S. radians and A. agaricites decreased to a lesser extent. Differences in the loss of algal cells on an aerial basis and in the cellular chlorophyll concentration were also found between these species. By combining the non-invasive PAM technique with whole-cell fluorescence of freshly isolated zooxanthellae, we have identified fundamental differences in the physiology of the symbionts within different species of coral. Zooxanthellae within M. annularis appear to be more susceptible to heat-induced damage at or near the reaction centre of Photosystem II, while zooxanthellae living in S. radians remain capable of dissipating excess excitation energy through non-photochemical pathways, thereby protecting the photosystem from damage during heat exposure.     

Oxidative stress causes coral bleaching during exposure to elevated temperatures

 Elevated temperatures and solar ultraviolet (UV) radiation have been implicated as recent causes for the loss of symbiotic algae (i.e., bleaching) in corals and other invertebrates with photoautotrophic symbionts. One hypothesized mechanism of coral bleaching involves the production of reduced oxygen intermediates, or toxic oxygen, in the dinoflagellate symbionts and host tissues that subsequently causes cellular damage and expulsion of symbionts. Measurements of photosynthesis in the Caribbean coral Agaricia tenuifolia, taken during temperature-induced stress and exposure to full solar radiation, showed a decrease in photosynthetic performance followed by bleaching. Exposure of corals to exogenous antioxidants that scavenge reactive oxygen species during temperature-induced stress improves maximum photosynthetic capacity to rates indistinguishable from corals measured at the ambient temperature of their site of collection. Additionally, these antioxidants prevent the coral from “ bleaching ” and affect the mechanism of symbiont loss from the coral host. These observations confirm a role for oxidative stress, whether caused by elevated temperatures or exposure to UV radiation, in the bleaching phenomenon. Accepted: 18 October 1996     

Superoxide Dismutase Is a Virulence Factor Produced by the Coral Bleaching Pathogen <Emphasis Type="Italic">Vibrio shiloi</Emphasis>

Coral bleaching is a disease that threatens coral reefs throughout the world. The disease is correlated with higher-than-normal seawater temperatures. Data have been reported showing that bleaching of the coral Oculina patagonica during the summer in the Mediterranean Sea is the result of an infection with Vibrio shiloi. The summer temperatures induce the expression of virulence factors in the pathogen. We report here that V. shiloi produces an extracellular superoxide dismutase (SOD) at 30°C, but not at 16°C. An SOD⁻ mutant was avirulent. The mutant adhered to corals, penetrated into coral cells, multiplied intracellularly for a short time, and then died. These data support the hypothesis that SOD protects the intracellular V. shiloi from oxidative stress caused by the high concentration of oxygen produced by intracellular zooxanthellae photosynthesis. Received: 3 July 2002 / Accepted: 27 July 2002     

Relationships among thermal stress, bleaching and oxidative damage in the hermatypic coral, Pocillopora capitata

To examine the response to exposure to a thermal gradient in coral, we assessed the effect of a gradual 10 degrees C temperature increase (22 to 32 degrees C over 10 h) on normal (N), partially bleached (P) and control (C) samples collected from different branches of the same coral (Pocillopora capitata). We examined markers of oxidative stress, including lipid peroxidation (MDA) and superoxide dismutase (SOD) activity, indicators of bleaching, including chlorophyll a (Chl a) and carotenoid pigment (PC) levels, as well as zooxanthellae density. Our results revealed that N, P and C coral samples all contained higher levels of PC versus Chl a. The levels of both pigments increased as the temperature increased from 22 to 28 degrees C only in N and C samples, whereas P samples showed less cellular damage than N and C samples at temperatures between 26 and 28 degrees C, and had greater antioxidant activities at temperatures between 26 and 30 degrees C. The rate of zooxanthellar expulsion consistently increased with temperature in all three coral types across the entire temperature range. Collectively, these results indicate that temperature has a direct effect on the antagonistic relationship between temperature-induced damage and protective antioxidant mechanisms in this type of coral.     

Differential Gene Expression in Symbiodinium microadriaticum Clade B Following Stress

Coral bleaching is caused by the loss of symbiont zooxanthellae and/or decrease in their pigments. Since the algal symbionts provide the energy basis for corals and whole reefs, their loss or impairment of function leads to widespread mortality. This phenomenon has been documented numerous times in recent years, and has extensively damaged coral reefs all over the world. Temperature has been found to be the major cause of bleaching, and rising sea temperatures have increased the frequency of these catastrophic episodes. To characterize the response of zooxanthellae to temperature stress at the molecular level, we used the mRNA differential display technique to monitor changes in the abundance of specific mRNA species in the cell under different temperature conditions. Axenically grown zooxanthellae were exposed to a range of temperatures (21.7, 17, 26°C) before extraction of their mRNA. Of numerous differentially expressed sequences, seven mRNA species were amplified by the polymerase chain reaction (PCR) and sequenced. One of those sequences was positively identified as encoding a multifunction cell surface aminopeptidase, dipeptidyl peptidase IV, which is active in cell matrix adhesion. Our work illustrates the power of the differential display technique as a useful tool to study the response of zooxanthellae to stressors.     

Atmospheric dimethysulphide production from corals in the Great Barrier Reef and links to solar radiation, climate and coral bleaching

Coral zooxanthellae contain high concentrations of dimethylsulphoniopropionate (DMSP), the precursor of dimethylsulphide (DMS), an aerosol substance that could affect cloud cover, solar radiation and ocean temperatures. Acropora intermedia a dominant staghorn coral in the Indo-Pacific region, contain some of the highest concentrations of DMSP reported in the literature but no studies have shown that corals produce atmospheric DMS in situ and thus could potentially participate in sea surface temperature (SST) regulation over reefs; or how production varies during coral bleaching. We show that A. intermedia from the Great Barrier Reef (GBR) produces significant amounts of atmospheric DMS, in chamber experiments, indicating that coral reefs in this region could contribute to an “ocean thermostat” similar to that described for the western Pacific warm pool, where significantly fewer coral reefs have bleached during the last 25?years because of a cloud-SST feedback. However, when Acropora intermedia was stressed with higher light levels and seawater temperatures DMSP production, an indicator of zooxanthellae expulsion, increased markedly in the chamber, whilst atmospheric DMS emissions almost completely shut down. These results suggest that during increased light levels and seawater temperatures in the GBR coral shut-down atmospheric DMS aerosol production, potentially increasing solar radiation levels over reefs and exacerbating coral bleaching.     

The adaptive bleaching hypothesis: experimental tests of critical assumptions

Coral bleaching, the loss of color due to loss of symbiotic zooxanthellae or their pigment, appears to be increasing in intensity and geographic extent, perhaps related to increasing sea surface temperatures. The adaptive bleaching hypothesis (ABH) posits that when environmental circumstances change, the loss of one or more kinds of zooxanthellae is rapidly, sometimes unnoticeably, followed by formation of a new symbiotic consortium with different zooxanthellae that are more suited to the new conditions in the host's habitat. Fundamental assumptions of the ABH include (1) different types of zooxanthellae respond differently to environmental conditions, specifically temperature, and (2) bleached adults can secondarily acquire zooxanthellae from the environment. We present simple tests of these assumptions and show that (1) genetically different strains of zooxanthellae exhibit different responses to elevated temperature, (2) bleached adult hosts can acquire algal symbionts with an apparently dose-dependent relationship between the concentration of zooxanthellae and the rate of establishment of the symbiosis, (3) and finally, bleached adult hosts can acquire symbionts from the water column.     

Bleaching of Hermatypic Corals

In this paper, I review data on the magnitude and extent of reef coral bleaching events and consider modern hypotheses on the mechanisms of this natural phenomenon and experimental data lying at their basis. Four possible mechanisms of color loss by hermatypic corals have been confirmed experimentally: bacterial infection, change of zooxanthellae type in the polyps to improve the heat resistance of the photosynthetic function of coral to elevated seawater temperature, intoxication of zooxanthellae by animal metabolic wastes at high temperature and light levels, and thermal and photodestruction of the animal and algal cells. The heating effect of photosynthetic active radiation on the zooxanthellar cells in coral polyps was verified theoretically. The calculations showed that in the natural environment, the additional light-induced heating of zooxanthellae is not above 0.01°C and that it cannot cause disruption of the animal and zooxanthellae symbiosis.     

THE EFFECT OF CONSTANT TEMPERATURES ON THE HATCHING OF EGGS AND SURVIVAL OF THE FRESHWATER SNAIL BIOMPHALARIA GLABRATA (SAY)

SUMMARY

The incubation period and percentage hatching of eggs of pigmented and unpigmented Biomphalaria glabrata at constant temperatures were investigated in the range 14 °C to 34 °C. In order to determine the influence of extreme temperatures on adult snails, specimens of the same species were exposed to 0 °C and 40 °C for selected time periods. The results indicate that sustained temperatures below 16 °C and above 32 °C are detrimental to the development and hatching of B. glabrata embryos. The optimum temperatures for incubation period and hatching differ from each other. As far as temperature is concerned, this foreign snail species should be capable of successfully colonizing the warmer parts of southern Africa.