PlantLife Volume 56.5, December 2023. Progress towards understanding the Blushing Bride Satyre species complex

 

A story of the Blushing Bride Satyre (Satyrium longicauda, Orchidaceae) species complex: Progress towards a better understanding

by Miguel Castañeda Zárate

The Orchidaceae family is one of the most charismatic plant families with species renowned for their diversity and beauty, both in colour and shape. Orchids are undoubtedly an interesting taxonomic group for amateur and professional botanists, horticulturists, collectors and traders. With about 26,000 species, Orchidaceae represents by far one of the most well-studied and best-known groups of plants (Figure 1). However, this number is constantly being updated as taxonomic novelties are discovered and described. For example, expeditions to under-explored areas, which have not received enough botanical attention, and even to well-botanised areas known to be floristically rich, can still result in the discovery of new species.

Additionally, the recognition of new “cryptic” species within “problematic” widespread species or species complexes is often possible through observations and thorough sampling of individual plants and populations. When highly variable species are thought to include two or more putative species they may be referred to as a species complex. Species complexes are taxonomically difficult and challenging to describe, potentially masking unidentified species with morphological (relating to physical structure or form) variation that is not well understood. The use of scientific tools that reveal differences and similarities not only in morphology and phenology but also in floral scent composition and molecular characteristics is important for understanding species complexes. Often the reassessment of species complexes leads to proposed taxonomic changes and usually results in splitting a single species into two or more biological entities (e.g., species, subspecies or varieties).

Figure 1. Several orchid species found in South Africa. Orthochilus foliosus (1.1), Cyrtorchis arcuata (1.2), Disa caffra (1.3), Satyrium trinerve (1.4), Disperis renibractea (1.5), Schizochilus bulbinella (1.6), Habenaria epipactidea (1.7) and Disperis fanniniae (1.8).

Back in 1800, the famous Swedish botanist and taxonomist Olof Peter Swartz described the terrestrial orchid genus Satyrium. This name originates from a Greek mythological creature Satyr, which is a demigod depicted as half man and half goat with horns on its head. The Satyr’s horns are a reference to the double spurs as described from the genus type species Satyrium bicorne (endemic to South Africa). The genus includes taxa characterised by having non-resupinate (non-inverted) flowers with two spurs projecting from the hooded labellum (Figure 2). Currently, over 90 species are accepted as part of the orchid genus Satyrium, which is not to be confused with the group of butterflies that share the same name. Most species occur in Africa, with a few in Madagascar and Asia.

Figure 2. Satyrium longicauda inflorescence and flowers, illustrating the spurs.

Forty-three species of Satyrium have been recorded in South Africa (Figure 3), of which 35 are considered endemic (restricted) to the country. In South Africa, Satyrium cristatum, S. longicauda, S. neglectum, and S. parviflorum represent examples of widespread species and/or highly variable species that conform to species complexes. Usually, these complexes have two or more recognised taxa below species level either as subspecies or varieties. The use of different sources of evidence (ecological, morphological, molecular, etc.) is likely to allow the description of many new species in years to come. Satyrium longicauda is an example of an intricate species complex with a high degree of morphological variation, not only in floral characteristics but also vegetatively. Here I will focus on this species complex within South African populations.

Figure 3. Examples of Satyrium species found in South Africa. S. rhodanthum (3.1) S. macrophyllum (3.2), S. sphaerocarpum (3.3) and S. longicauda (3.4).

Commonly known as the Blushing Bride Satyre, S. longicauda was described in 1838 by John Lindley, based on a specimen collected in the Eastern Cape, South Africa. Lindley named this species in reference to the characteristic long spurs (cauda = tail). Satyrium longicauda is a common element of grasslands in the summer rainfall regions of the Eastern Cape, KwaZulu-Natal, Free State, Mpumalanga, and Limpopo Provinces. Nevertheless, the species does not exclusively occur in South Africa but can also be found in other eastern and southern African countries. This species bears white flowers that sometimes have a light to dark pink or even reddish tinge. To attract pollinators, the flowers produce a sweet scent that is released at dusk and offers nectar as a reward in the spurs. Traditionally, S. longicauda has been divided into two varieties, var. longicauda and var. jacottetianum, accounting for differences in the length of their floral components, particularly the lateral sepals and spurs (Figure 4). The variety jacottetianum has spurs 13–26 mm long and lateral sepals 4–7 mm long whereas variety longicauda has spurs 24–46 mm long, and lateral sepals 5–11 mm. An interesting fact is that not only are these varieties considered to be part of the complex but the complex also includes the species S. buchananii (not distributed in South Africa) and S. rhodanthum (endemic to KwaZulu-Natal). Despite these species showing affinities with S. longicauda, more detailed studies are required to provide a complete taxonomic interpretation. For now, let’s focus on the actual Long-tailed Trewwa, another name given to the species of interest. 

Figure 4. Satyrium longicauda var. jacottetianum (4.1) and S. longicauda var. longicauda (4.2)

After studying 60 natural populations mainly from KwaZulu-Natal, South Africa, I was able to provide a better interpretation of the wide variation observed in the species. All populations that I had the opportunity to visit were sampled during the flowering period of September–April. To interpret the complex, visual observation played a crucial role in the detection of characteristic differences in the individuals, i.e. plant and flower size, flower colour, leaf number and position, as well as microhabitat and type of pollinator. Together, these characteristics revealed the presence of eight morphological variants that I called morphotypes either co-occurring or isolated. I was able to identify two main groups based on vegetative characteristics, morphotypes with one or two leaves that were either flat on the ground or erect (Figure 5). Within these two groups, there were short and tall plants with white or pink- to reddish-tinged flowers growing either in dry or wet sites. I also noted the pollinators: seven out of eight morphotypes are pollinated by nocturnal moths but surprisingly I found that one was pollinated only by an oil-collecting bee (more about this below). For the quick identification of these morphotypes, I decided to name them according to their characteristics: OELB = one erect leaf bee; OELM = one erect leaf moth; OFL = one flat leaf; OFLD = one flat leaf dwarf; TELW = two erect leaves wetland; TFLD = two flat leaves dwarf; TFLP = two flat leaves pink and TSLG = two spreading leaves giant.

 

Figure 5. Examples of leaves observed on two of the morphotypes of the Satyrium longicauda complex - one flat leaf (5.1 and 5.2) and two fleshy leaves giant (5.3 and 5.4)

For example, at one of my field sites, the Umtamvuna Nature Reserve (located on the south coast of KwaZulu-Natal), I discovered that three morphotypes, OELM, TELW and TSLG, occurred in the Reserve, each with a partial difference in flowering time (Figure 6). Having these initial groupings took me to the next step, recording measurements of flowers and vegetative structures, such as flower colour, number of flowers, spur length and the number and position of the leaves. It was determined that TELW usually bears fewer flowers compared to OELM and TSLG. Another interesting fact was that TELW always occurs in marshes whereas OELM and TSLG always grow in close proximity to each other in drier soils, both in open grasslands. Lastly, TELW starts flowering earlier in the season (mid  September – mid October) and it is followed by OELM (late September – late October) and TSLG (late October – November) respectively. 

Figure 6. View of the Umtamvuna Nature Reserve (6.1) and inflorescences of the Satyrium longicauda morphotypes present TELW (6.2), OELM (6.3) and TSLG (6.4)

The pollinators of these morphotypes were recorded using camera traps and direct observations at dusk (Figure 7). To identify the pollinators, insect visitors were captured and inspected for pollen on their proboscis (tongue-like structure), confirming that they were indeed the pollinators and not nectar robbers. All three morphotypes are visited and pollinated at night by moths (Figure 7), which are attracted by the sweet scent of the flower to the nectar rewards. Although I sampled the perfume produced by the flowers from the three morphotypes, I did not find any clear scent differences (Figure 8). By using morphometrics (quantitative analysis of size), I corroborated what could be easily seen, that there was a large overlap in morphology. Nevertheless, each morphotype exhibited distinct morphological characters including spur length, leaf number and position. The combination of evidence from the morphology, flowering phenology, and genetics (at least in part) separated them into individual morphotypes.

Figure 7. Camera trapping set up in the Umtamvuna Nature Reserve to record moth pollinators visiting the orchids (7.1). The hawkmoth Bassiothia schenkii pollinating the TSLG morphotype of the Satyrium longicauda complex (7.2)

 

 Figure 8. Satyrium longicauda floral scent sampling.

I would like to conclude by stressing that the number of species within the Satyrium longicauda complex may be greater than we currently realise. It is possible that the addition of more populations not only from the central area of distribution of South Africa but from the northern and southern distribution as well as other countries, will achieve a more complete understanding of the already described morphotypes. Other morphotypes may also be found. Potentially, morphotypes may even be recognised as different species. In fact, I recently described S. cernuiflorum (Figure 9), a species that could be considered part of var. jacottetianum for its short spurs (6.6–24.1 mm). However, Satyrium cernuiflorum is characterised by having a single erect leaf with scented white flowers usually facing downwards that offer oil rather than nectar to its pollinators. The oil is gathered during the daytime by female oil-collecting bees, Rediviva neliana (Figure 9). This species has short spurs compared to TELW and TSLG.

Figure 9. Satyrium cernuiflorum from KwaZulu-Natal. From left to right: S. cernuiflorum being pollinated by the oil collecting bee Rediviva neliana (9.1). Inflorescence with slightly curved flowers (9.2). Inflorescence with deeply curved flowers (9.3). Single erect leaf (9.4). Individual showing the characteristic single erect leaf (9.5). Reproductive individuals at the type locality (9.6).

On a final note, if you stumble across S. longicauda in the field, I strongly encourage you to take note of leaf shape, size, number and position (Figure 10), and not only the beautiful, pleasantly scented inflorescences that catch our attention, as this adds important information for its identification.

Figure 10. Leaf variation in Satyrium longicauda morphotypes.  One flat leaf (OFL) (10.1), one erect leaf moth (OELM) (10.2), two erect leaves wetland (TELW)(10.3) and two spreading leaves giant (TSLG) (10.4).

References

Castañeda-Zárate M, Johnson SD, van der Niet T. 2021. Food reward chemistry explains a novel pollinator shift and vestigialization of long floral spurs in an orchid. Current Biology 31: 238–246.e7.

Castañeda-Zárate M, Johnson SD, van der Niet T. 2022. Description of a new species within the Satyrium longicauda (Orchidaceae) complex from South Africa, based on integrative taxonomy. South African Journal of Botany 148: 379–386.

Castañeda-Zárate M, Bytebier B, Johnson SD, van der Niet T. 2022. Satyrium cernuiflorum, a new name for Satyrium cernuum Castañeda-Zárate & van der Niet (Orchidaceae). South African Journal of Botany 150:13.

Castañeda-Zárate M, Johnson SD, van der Niet T. 2023. Widespread coexistence of genetically distinct morphotypes in the Satyrium longicauda complex (Orchidaceae). Botanical Journal of the Linnean Society 202 (3):406–431.

Hall A. 1982. A revision of the southern African species of Satyrium. Contributions from the Bolus Herbarium 10: 1–137.

Johnson SD, Peter CI, Ellis AG, Boberg E, Botes C, van der Niet T. 2011. Diverse pollination systems of the twin-spurred orchid genus Satyrium in African grasslands. Plant Systematics and Evolution 292: 95–103.

Kurzweil H, Linder HP. 1999. A phylogenetic analysis of the genus Satyrium (Orchidaceae). Beiträge zur Biologie der Pflanzen 71: 101–181

About the author: Miguel Castañeda Zárate is a biologist with over 15 years studying plants, particularly orchids. He recently obtained his PhD at the University of KwaZulu-Natal. He loves botanising and enjoys going on long hikes in search of flora, especially orchids.