Protomelas krampus, a new paedophagous cichlid from Lake Malawi (Teleostei, Cichlidae)

Abstract. A new paedophagous species of Protomelas, P. krampus sp. nov., is described from Lake Malawi. It has been found in Lukoma Bay in Tanzania, near Mara Point in Mozambique, and at Otter Point, Chizumulu, the Likoma Islands and Mazinzi Reef in Malawi. This species is placed in the genus Protomelas based on its melanin pattern, which comprises a continuous midlateral stripe. A morphometric study was done to compare this species with its congeners and similar species of Hemitaeniochromis and Caprichromis. It differs from most congeners by having only one inner tooth row. Furthermore, P. krampus sp. nov. differs from P. insignis, P. spilopterus, H. brachyrhynchus, H. urotaenia, Caprichromis liemi and C. orthognathus by its shorter premaxillary pedicel, shorter prepectoral distances and dentition. It also differs largely in its melanin pattern from the paedophagous species C. liemi, C. orthognathus, Diplotaxodon greenwoodi and Naevochromis chrysogaster, as well as H. brachyrhynchus and H. urotaenia. Protomelas krampus sp. nov. has been observed to ram mouth-brooding cichlids from above to feed on their eggs or larvae.


Introduction
Lake Malawi is home to about 800 to 1000 species of endemic cichlids (Snoeks 2000;Konings 2016). Because of their explosive speciation, species can be difficult to delineate and many species complexes and genera still need to be taxonomically resolved.
Three confirmed paedophagous species have currently been described from Lake Malawi. Protomelas spilopterus has short, oblique jaws with thick gums and one or two inner tooth rows. Both Caprichromis liemi and C. orthognathus have a melanin pattern with a diagonal stripe running from the nape to the base of the caudal fin. The teeth on the lower jaw are embedded in thick gums. Especially C. orthognathus has a steeply inclined mouth (Eccles & Trewavas 1989;Konings 2016). In addition to P. spilopterus, C. liemi and C. orthognathus, two more species are suspected of having a paedophagous diet (Stauffer & McKaye 1986;Eccles & Trewavas 1989). Diplotaxodon greenwoodi Stauffer & McKaye, 1986 is a widespread deep-water species. The genus Diplotaxodon Trewavas, 1935 is characterized by the lack of distinct markings such as bars or spots on the body. Its lower jaw protrudes and the teeth on the lower jaw are embedded in thick gums. Diplotaxodon greenwoodi has a steeply inclined mouth, large eyes and one to three inner tooth rows (Stauffer & McKaye 1986;Trewavas & Eccles 1989;Snoeks 2004). Naevochromis chrysogaster (Trewavas, 1935) has a suprapectoral spot, a midlateral spot covering the lateral line, a supranal spot positioned between the lateral lines and a precaudal spot. The chin is prominent and thick. It has a broad mouth and fleshy lips that embed the teeth. There is one inner row of teeth in the upper and two in the lower jaw (Eccles & Trewavas 1989;Konings 2016).
As is clear from various discussions (e.g., Eccles & Trewavas 1989;Snoeks 2004;Oliver 2012;Konings 2016) there is still some confusion regarding the classification of species within the genera Protomelas DIERICKX K. & SNOEKS J., A new paedophagous cichlid 3 and Hemitaeniochromis. In this study, we follow the classification provided by Eccles & Trewavas (1989), expanded by Oliver (2012). It is, however, clear that a taxonomical revision of the species in the genera Protomelas and Hemitaeniochromis is necessary. For now, we suggest including the newly described paedophagous species in the genus Protomelas based on its continuous midlateral band and short jaws, following Snoeks & Hanssens (2004). We await a further revision of the complex for a final generic allocation. Below, the species that is new to science is described as Protomelas krampus sp. nov.

Material and methods
In total, 44 specimens of Protomelas, Hemitaeniochromis and Caprichromis in the collections at the Royal Museum of Central Africa, Tervuren, and the Natural History Museum, London, were examined: five specimens of C. liemi, five of C. orthognathus, one of H. brachyrhynchus, five of H. urotaenia, eleven of H. sp. 'insignis like' (sensu Snoeks & Hanssens 2004), four of P. insignis, two of P. krampus sp. nov. and eleven of P. spilopterus.
The measurements and counts performed here follow Snoeks (2004). Two additional measurements, as described by Oliver (2012), were taken: the snout width and belly length. Also, the gape inclination, the angle between the midlateral line and the anteriormost tip of the upper jaw, was measured. In total, 21 length measurements, 13 counts (including the number of vertebrae via X-rays), one angle (gape inclination) (see Tables 4 and 5) and some qualitative observations on the body and head shape, dentition, and the colour pattern in alcohol were made.
Principal component analysis (PCA) was performed in Past3 (Hammer et al. 2001) to explore the multivariate data set. Measurements were log-transformed and the covariance matrix was used. When using log-transformed measurements, the individual loadings of all variables on the first principal component (PC 1) are of the same magnitude and sign, and PC 1 can therefore be regarded as a proxy for multivariate size (Jolicoeur 1963;Snoeks 2004;Van Steenberge et al. 2015). The correlation matrix was used for the raw meristic data.

Comparative morphometrics
A PCA on 21 log-transformed measurements including all specimens showed a clear separation of Protomelas krampus sp. nov. from all other species in the negative part of PC 2 on the second principal axis (Fig. 1). In general morphology, it seems to be most similar to C. orthognathus. The most important loadings on PC 2 are of the premaxillary pedicel length, cheek depth, belly length, caudal peduncle length, interorbital width and dorsal fin base (Table 1). In a comparison with both species of Caprichromis, P. krampus sp. nov. remains clearly separated on the third principal axis (Fig. 2). The most important  6 loadings on PC 3 are for the premaxillary pedicel length, the interorbital width, the snout length, the head width, the dorsal fin base and the snout width (Table 2).
In a PCA on the raw meristics, the picture was less clear. Still, P. krampus sp. nov. was separated from all other species (Fig. 3), mostly on PC 1. The most important loadings on PC 1 are of the number of vertebrae, the number of both upper and lower jaw teeth, the number of longitudinal line scales, the  number of dorsal fin spines and the number of anal fin rays. On PC 2, the highest loadings are the number of dorsal fin rays, the number of anal fin rays, the number of scales on the lower lateral line, the number of longitudinal line scales, the number of pectoral fin rays and the number of outer lower jaw teeth (Table 3).  (Trewavas, 1935), P. kirkii (Günther, 1894), P. labridens (Trewavas, 1935), P. macrodon Eccles, 1989, P. marginatus (Trewavas, 1935, P. pleurotaenia (Boulenger, 1901), P. similis (Regan, 1922), P. spilonotus (Trewavas, 1935), P. taeniolatus (Trewavas, 1935), P. triaenodon (Trewavas, 1935) and P. virgatus (Trewavas, 1935), by having only one inner tooth row, whereas the other species have two rows. Protomelas krampus sp. nov. differs from Diplotaxodon greenwoodi by the lack of a melanin pattern in the latter species. It has isognathous jaws, whereas D. greenwoodi has a protruding lower jaw.

Taxonomy
Protomelas krampus sp. nov. differs from Naevochromis chrysogaster by its melanin pattern, which consists of three large spots on the lateral sides in the latter instead of a continuous midlateral line. It has a more strongly inclined gape than N. chrysogaster. Protomelas krampus sp. nov. has only one inner tooth row on the lower jaw, whereas N. chrysogaster has two.

Etymology
The specific name, ʻkrampusʼ, is a noun in apposition and was chosen in reference to the European folklore character Krampus. This demon puts naughty children in a bag and takes them away, which is reminiscent of a paedophagous behaviour. The goat-like appearance of Krampus also implicitly refers to the head-butting behaviour of the species. The same implicit reference to this behaviour is also found in the genus name Caprichromis of other paedophagous species of Lake Malawi.

Description
Based on holotype and one paratype (see Figs 4-5 and Tables 4-5). Qualitative observations are described in the context of Lake Malawi haplochromine cichlids as conducted by Snoeks (2004).
TeeTH. Outer row of teeth on upper and lower jaws mostly unequally bicuspid and some posterior teeth unicuspid in smaller specimen; anterior teeth exclusively unicuspid on both jaws of larger specimen. Teeth straight and not curved inwards. Anterior cusps of teeth on outer row in both jaws larger than posterior cusps in smaller specimen. Anterior teeth larger than posterior teeth in smaller specimen. One inner row of irregularly placed tricuspid teeth on both jaws in smaller specimen. Posterior and inner teeth in larger specimen not readily observable, being to a large extent or fully covered by fleshy gums. Teeth closely set (space between teeth about half to one tooth width).
Fins. Pectoral fin origin behind level of dorsal fin origin in smaller specimen. Position of pectoral fin origin unknown in larger specimen because of damage. Pelvic fin origin positioned slightly more backwards than level of dorsal fin origin. Pectoral fin of holotype and pelvic fin in both types almost to level of anus. Anal fin anterior to level of first soft dorsal fin ray. Small scales on base of caudal fin rays.

Colour pattern in life
Based on a photograph by Konings (2016) (Fig. 6). Body generally greyish. Head and pectoral fin base yellowish. Pelvic fin with white distal part of leading edge. Five orange-brownish eggspots on anal fin. Continuous dark midlateral band from about one eye length behind opercle to caudal fin. Supralateral row of darks spots. Dark spots also present just below dorsal fin. Some spots are arranged in an interrupted vertical bar pattern. Fig. 7. Distribution map of Protomelas krampus sp. nov. Red star = holotype; red dot = paratype; green triangles = possible sightings by Konings (2016); orange square = possible sighting by McKaye & Kocher (1983); yellow diamond = possible sighting by Stauffer (pers. comm.). Inset: map of Africa with indication of area of Lake Malawi.

Colour pattern in preserved specimens
Based on photographs by McKaye & Kocher (1983) and Snoeks (2004) (Fig. 5). Body generally brown or greyish. Dorsum somewhat darker than belly. Darker on dorsal parts of head and body contiguous with dorsal fin base. Clear dark maculae on spiny part of dorsal fin, possibly also on soft dorsal fin part and caudal fin. Continuous dark midlateral band from one eye length or about three scales behind opercle to caudal fin. One supralateral and one subdorsal row of darks spots. Some spots as subtle, incomplete vertical bars. Both types currently pale-coloured, probably due to light exposure (Fig. 4).
Geographical distribution (Fig. 7) of the head. When the chin is enlarged, it is easier to use it as a ram from this orientation and possibly to have more impact on the snout of the prey. This may also explain the large gape inclination. The different angle of attack and slight differences in morphology may be explained by niche partitioning (McKaye & Kocher 1983). The precise phylogenetic relationships between the paedophagous species should, however, be further studied with genetic analyses and a thorough taxonomic revision.
During our analyses, it became clear that there may be an additional undescribed species within the genus Protomelas. The lectotype of P. spilopterus and one paralectotype (tag 2583 within BMNH 1935.6.14.652-657) differ from the other paralectotypes in several features. The head of these two specimens is steeper and the neurocranial crest appears to be more rounded. They show a clear chin, whereas the other paralectotypes lack a chin. The jaws of the lectotype and some paralectotypes are rounded, while the others have wide and anteriorly flattened jaws. The lacrimal appears to be somewhat larger and has a more rounded anterior side in the lectotype and paralectotype compared to the other paralectotypes. The caudal fin of the lectotype and paralectotype is emarginate, whereas the other paralectotypes of P. spilopterus have a truncate caudal fin with a longer dorsal lobe than ventral lobe. Furthermore, the lectotype has bicuspid teeth, the second cusp of which is very small, in the outer row on both jaws, and a mixture of uni-and tricuspid teeth on the two inner rows. Its teeth are curved inwards. The teeth of all paralectotypes are angled forwards and are uniquely unicuspid and conical, and there is only one inner tooth row on both jaws. The deepest point of the body occurs at the level of the pectoral fin origin in the lectotype and posterior to the pectoral fin origin in most paralectotypes. The eggspots on the anal fin of the lectotype are placed in three rows: the distal row with seven spots, the middle row with three spots and one spot in the proximal row. Only one other paralectotype has eggspots in two rows with five spots on the distal row and four or five spots on the proximal row. A more detailed study is necessary to assess whether or not the type series is polyspecific.