A Tentative Review of Sexual Behavior and Alternative Reproductive Strategies of the Italian Colubrid Snakes (Squamata: Serpentes: Colubridae)

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Zeitschrift/Journal: Herpetozoa

Jahr/Year: 1997

Band/Volume: 10_3_4

Autor(en)/Author(s): Capula Massimo, Luiselli Luca M.

Artikel/Article: A tentative review of sexual behavior and alternative reproductive strategies of the Italian colubrid snakes (Squamata: Serpentes: Colubridae). 107-119 ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at

HERPETOZOA 10 (3/4): 107 -119 Wien, 30. Dezember 1997

A tentative review of sexual behavior and alternative reproductive strategies of the Italian colubrid snakes (Squamata: Serpentes: Colubridae)

Versuch einer Zusammenschau über das Sexualverhalten und alternative Fortpflanzungsstrategien der Nattern Italiens (Squamata: Serpentes: Colubridae)

MASSIMO CAPULA & LUCA LUISELLI

KURZFASSUNG

Die vorliegende Arbeit gibt einen Überblick über das Fortpflanzungsverhalten der Nattern Italiens unter beson- derer Berücksichtigung von Männchen-Männchen-Kämpfen um den Zugang zu fortpflanzungsfähigen Weibchen sowie von alternativen Fortpflanzungsstrategien. Wir diskutieren (i) die verfügbaren Literaturdaten, stellen (ii) Origi- naldaten über wenig bekannte Arten vor und machen (iii) den Versuch einer vorläufigen Typisierung dieser Kämpfe zwischen männlichen Colubriden Italiens. Danach lassen sich vier Typen von Kämpfen unterscheiden, wobei Beißen nur bei ungiftigen Schlangen vorkommt. Die Kämpfe fuhren in der Regel nicht zur Beschädigung der Beteiligten, doch wird für Elaphe situla ein Fall mit fatalem Ausgang berichtet Kämpfe zwischen Männchen wurden bei 13 der 19 Schlangenarten Italiens (68,4%) festgestellt und bisher an 21 Populationen untersucht Diese Prozentangabe ist wahr- scheinlich korrekturbedürftig, da Angaben zu drei sehr seltenen Arten nicht verfügbar sind. Nur bei der Gattung Natrix scheinen Kommentkämpfe nicht vorzukommen, doch könnten bei N. natrix physische Interaktionen zwischen Männchen, die gleichzeitig um ein einzelnes Weibchen werben, zu einer Art "Pseudokampf führen, in dem die Größe des Männchens für seinen individuellen Fortpflanzungserfolg bedeutsam sein kann. Im Dienste der Fortpflanzung ste- hende Kämpfe fanden sich bei Schlangenarten, in denen die Männchen größer sind als die Weibchen (n = 3), ebenso wie bei Arten ohne ausgeprägten sexuellen Größendimorphismus (n = 4) und bei Arten mit größeren Weibchen (n = 4). Die Analyse zeigt einen Zusammenhang zwischen Sexualdimorphismus mit größeren Männchen und dem Auftre- ten von Kämpfen sowohl bei den Colubriden Italiens als auch bei Schlangen im allgemeinen (SHINE 1978, 1993, 1994). Kämpfe ließen sich bei 100% der lebendgebärenden Taxa (inklusive Viperiden: n = 5 Arten), jedoch nur bei 72,7% der oviparen Formen nachweisen. Bei einigen Arten zeigten sowohl alpine als auch mediterrane Populationen diese sozialen Verhaltensweisen. Herbstpaarungen, Frühjahrsgeburten und Langzeit-Samenspeicherung wurden bei den Nattern Italiens nur selten beobachtet.

ABSTRACT

In this paper data on the reproductive behavior of the Italian colubrid snakes are reviewed, with an emphasis on the occurrence of male-male combats for the access to reproductive females, and on the occurrence of alternative reproductive strategies. We (i) discuss the data available in the literature, (ii) include original information on the most unknown species, and (iii) give a tentative "classification" of the behavioral types of male combats exhibited by the colubrids of the Italian Peninsula. Four types of sexual combats were identified, but biting is present only in non- venomous species. Combats were generally harmless to the rivals, but a case of fatal combat is reported for Elaphe situla. Sexual fights among males were seen in 13 out of the 19 Italian snake species (68.4%), and studied in 21 dif- ferent populations to date. This proportion should probably be retouched as we had no available information on three very rare species. The sole taxa that seem to lack sexual fights are those of the genus Natrix, but in N. natrix some physical interactions between males simultaneously courting single females may lead to a kind of "pseudocombat" where male body size is important for increasing the individual reproductive success. Sexual combats were found in snake species where males are bigger than females (n = 5), in species with no significant sexual size dimorphism (n = 4), and in species with females bigger than males (n = 4), but, examining the data in more detail, it turned out that male-larger dimorphism and occurrence of sexual combats are correlated in Italian colubrids, as well as in snakes in general (SHINE 1978, 1993, 1994). Sexual combats were omnipresent in the live-bearing taxa (vipers included: n = 5 species, 100% of.the cases), but were present in 72.7 % of the oviparous ones. In some species these social behaviors were exhibited both by alpine and Mediterranean populations. Autumnal mating, spring births, and long-term sperm storage were rarely observed amongst Italian colubrids.

KEY WORDS

Serpentes, Colubridae; Natrix maura, N. natrix, N. tessellata, Coluber gemonensis, C. viridiflavus, Coro- nella austriaca, C. girondica, Elaphe longissima, E. quatuorlineata, E. scalaris, E. situla, Macroprotodon cucullatus, Malpolon monspessulanus, Telescopus fallax; behavior, reproductive biology, sexual competition, combats, alternative mating strategies, long term sperm storage, autumnal mating, spring births; Italy. ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at

108 MASSIMO CAPULA & LUCA LUISELLI

INTRODUCTION

In recent years the available data on sexual dimorphism and male combats in snake reproductive biology and mating snakes, SHINE collated data from 374 taxa systems has expanded enormously, and the of eight families, but scarcely presented the comparative analysis of this large data- European forms. This becomes evident body has produced vigorous improvement when we examine the snake fauna of the in our knowledge (e.g., SHINE 1978, 1994). Italian Peninsula: although it includes 19 For instance, it is now clear that male-male species from two families (4 viperids and combats are important components of the 15 colubrids), SHINE (1994) was only able reproductive biology of many snake spe- to list 9 species (47.3% of the total), but cies, while less than twenty years ago these none of the papers reviewed by him was agonistic behaviors were known in 5.5% of specifically concerned with Italian popula- the genera and in less than 2% of the tions of snakes. However, several Italian known species only (CARPENTER 1977a). snake populations have been subject to ac- The secretive habits of most snakes curate field-research in recent years (e. g., cause strong constraints to field research CIOFI & CHELAZZI 1991, 1994; CAPULA & (SEIGEL 1993), and this has resulted in that LUISELLI 1994; LUISELLI 1995,1996). we only know in detail the components of Aim of this paper is to collate data on the reproductive biology of a few (less se- the reproductive behavior of the Italian cretive or very common) species, while colubrid snakes, focusing on male combats there are still so many species that we and alternative mating strategies. We dis- know very little about. As for the European cuss the data available in the literature, but species, a large body of eco-ethological also include original information on the studies is available for species such as the most unknown species. Our attention has Adder Vipera berus (for a recent review see been focused on (1) the occurrence of male- LUISELLI 1995), Smooth Snake Coronella male combats for access to females and its austriaca (SPELLERBERG & PHELPS 1977; relation to sexual size dimorphism and op- GODDARD 1981; GENT 1988; ANDREN & erational sex-ratio; (2) the main character- NILSON 1992; LARSSON 1994; LUISELLI & istics of reproductive phenology (e. g., du- al. 1996) and Grass Snake Natrix natrix (e. ration of mating season etc.); and (3) the g., MADSEN 1983, 1984, 1987; MADSEN & potential for long-term sperm storage and SHINE 1993a, 1993b; LUISELLI 1996; LUI- other alternative reproductive strategies to SELLI & al., 1997), while the information occur. We also give a tentative "classific- on other widespread taxa (e. g., Elaphe si- ation" of the behavioral types of male com- tula, Telescopus fallax, Coluber viridifla- bats exhibited by the snakes of the Italian vus) is very sparse and anecdotal. This dis- Peninsula. In order to highlight all of these proportionate knowledge is clearly ex- points, we will systematically account on pressed by some recent reviews of snake every colubrid snake species of the Italian behavioral biology, such as those of SHINE fauna. (1993, 1994). In his exhaustive reviews on

MATERIALS AND METHODS The data presented here comes from are presented in table 1. In the following both literature papers and original obser- text the term "sexual size dimorphism" is vations. The latter were done both in cap- abbreviated by SSD. tivity and in the field, especially in two re- To give a preliminary "classification" gions where long-term researches on snake of the behavioral types of male combats behavior have been conducted: (i) a Medi- exhibited by the snakes of the Italian Pen- terranean hilly site in central Italy - Tolfa insula, we subdivide male combats into Mountains, province of Rome, and (ii) an four groups: type (1): highly ritualized dan- alpine mountainous site in northeastern It- ces without biting (Vipera type, see SAINT aly - Tarvisio Forest, Carnic Alps, province GIRONS 1947; ANDREN 1986); type (2): of Udine. The sources of all observations combats based on vigorous biting (as in ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at

Sexual behavior in Italian colubrìds 109

many Lampropeltis, see CARPENTER 1986); tion in nature, (ii) terrarium experiments type (3): combats based on both vigorous may be not representative of the natural biting and tail wrestling (as in Coronella situation, and (iii) the quantitative descrip- girondica; see below); type (4): combats tion of the agonistic behaviors needs to be ritualized with occasional biting. This very accurate (for excellent examples see classification is merely tentative, as (i) it is ANDREN 1986; SCHUETT & GILLINGHAM very difficult to observe the sexual combats 1989), and goes much beyond the scope of from beginning to the end of the interac- this article.

RESULTS The knowledge on the reproductive very local scale which is not ideal for field biology and behavior of the Italian colu- studies. brids is generally less than that of the Ital- At an extremely detailed level we ian vipers. This is due to (1) the obvious know the reproductive biology of one al- argument that venomous snakes capture pine population of Coronella austriaca the attention of scientists more than the (LuiSELLi & al. 1996) and of both alpine non-venomous ones, (2) the more secretive and Mediterranean populations of Natrix habits of most colubrids in comparison natrix (LuiSELLi 1996a; LUISELLI & al. with the viperids, (3) the lower site-fidelity 1997). The reproductive behaviors of the of the colubrids which causes strong prob- other species are less well known, and the lems to field research, and (4) the low available data is very poor. density of most colubrid populations at the

Male-male competition and mating behavior: A systematic account The data on the occurrence of male- "electrically" move around the copulating male competition, body sizes of the two pair, thus disturbing the action of the mat- sexes, and reproductive mode is summa- ing couple by a series of tail and body rized in table 1. movements. Lf the mating pair continues Natrix: Three species belonging to copulation despite the other males distur- this genus are found in Italy; all are ovipa- bance, the sexual agitation of the other rous, semi-aquatic, and with female-larger males begins to decrease, and the copulat- SSD. Coloration of males and females is ing pair is usually abandoned within some nearly identical in each species. minutes (MADSEN & SHINE 1993a; LUI- Grass Snakes - Natrix natrix (LIN- SELLI 1996). NAEUS, 1758) are known for frequently for- In the eastern Alps (Tarvisio Forest, ming "mating balls" during the reproduc- province of Udine, about 1100 m a.s.l), the tive season (BRUNO & MAUGERI 1990; mating season is short (2-3 weeks on aver- MADSEN & SHINE 1993a). When several age, from mid-May to early June) and ex- males simultaneously court one female, plosive: since not all the females emerge their tails frequently and vigorously inter- from hibernation on the same day, the daily act with each others, and the larger indi- operational sex-ratio is strongly skewed to viduals often drive away the tails of the males (which emerge from hibernation smaller rivals (MADSEN & SHINE 1993a; earlier than the females), so that it is easy LUISELLI 1996). These "electric" gregarious to see four or five individuals simultane- courtships may last for a very variable time ously courting a single female (LUISELLI & (sometimes for more than one hour) until al. 1997). In Mediterranean central Italy one of the males becomes able to insert a (Tolfa Mountains, province of Rome, about hemipenis into the female cloaca; the fe- 250-450 m a.s.l) the operational sex-ratio male, however, is not passive in this con- is equally skewed, but the mating season is text (LUISELLI 1996). Immediately after the much more prolonged (at least 5 weeks), beginning of the successful copulation, the and as a consequence, the mating "balls" other males in the swarm continue to are usually formed by a lower number of ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at no MASSIMO CAPULA & LUCA LUISELU

Table 1: Occurrence of sexual combats, sexual size dimorphism and mode of reproduction in various populations of Italian snakes according to literature and original data. Information from only Italian populations is given. Types of combat: 1: ritualized dance without biting (Vipera berus type); 2: combat based on vigorous biting; 3: combat based on vigorous biting and tail wrestling; 4: combat ritualized with occasional biting. Mean adult total lengths (TL) are given for males and females (m / 0 and are expressed in cm. When total lengths were not available from literature, the approximate averages found by us during our field trips are given. Some species appear more than once because data are available from more than one source. The symbol (!) indicates our unpublished observations. When the observations are original, the geographic position and the climate of the area where these data were obtained are given. Tab 1 : Auftreten von paarungsbedingten Kämpfen zwischen Männchen und sexuellem Größendimorphismus sowie Fortpflanzungsmodus in verschiedenen Schlangenpopulationen Italiens auf Grundlage von Literaturangaben und Originaldaten. Angaben beziehen sich nur auf italienische Populationen. Typisierung der Kämpfe: 1: Ritualisierter Tanz ohne Beißen (Vipera berus Typ); 2: Kampf mit heftigem Beißen; 3: Kampf mit heftigem Beißen und Ringen; 4: Ritualisierter Kampf mit gelegentlichem Beißen. Mittlere Ge- samtlängen (GL) von adulten Männchen und Weibchen (m / w) sind in cm angegeben. Wo solche Längen aus der Lit- eratur nicht verfügbar waren, wurden entsprechende Werte aus unseren Felduntersuchungen angegeben. Arten er- scheinen mehrmals in der Tabelle wenn Daten aus mehr als einer Quelle verfugbar waren.. Ein Rufzeichen (!) bezeichnet eigene unpublizierte Angaben. Bei solchen Originalangaben ist die geographische Lage angegeben und das Klima des Untersuchungsgebietes charakterisiert. A • [Tolfa Mountains, about 300 m a.s.l., Mediterranean climate], B • [Carnic Alps, about 1100 m a.s.l., alpine climate], C • [observations on captive animals from Croatian coast, about 20 m a.s.l.], D • [Central Apennines, about 800 m a.s.l., Subcontinental climate], E • [Roman Country, 100 m a.s.l., Mediterranean climate], F - [central and southern Italy, Mediterranean climate], G - [Salento, about 50 m a.s.l., Mediterranean climate], H - [observations in captivity from animals of Lampedusa, Mediterranean climate].

Species Combat Type Reprod. mode Mean TL (m / f) Locality Reference Art Kampf Typ Reprod.-modus Mittlere GL (m / w) Ort Quelle

Natrix maura no - ovip. 45.5 / 55.5 BRUNO (1984) Natrix natrix no ovip. 84.3 / 99.7 A LUISELU (1996) Natrix natrix no ovip. 68.5 / 82.5 B (!) Natrix tessellata no . ovip. 62.2 / 78.5 A FILIPPI (1995) Coluber hippocrepis ? ? ovip. 115 / 90 Coluber\gemonensis yes 1 ovip. 110 / 90 0) Coluber viridiflavus yes 1 ovip. 125 / 105 Coluber viridiflavus yes 1 ovip. 121 / 117 (!) Coronella austriaca yes 2 vi vip 51.1 / 48.7 Coronella girondica yes 3 ovip. 52.4 / 50.8 Elaphe longissima yes 1 ovip. 110.3 / 106.5 Elaphe longissima yes 1 ovip. 116 / 102 Elaphe quatuorlineata yes ? ovip. POZIO(1976) Elaphe quatuorlineata yes 4 ovip. 130 / 155 Elaphe situla yes 4 ovip. 70 / 90 Elaphe scalaris ? ? ovip. 85 / 120 Macroprotodon cucullatus yes 2 ovip. 45 / 45 Malpolon monspessulanus yes 1 ovip. 130 / 90 FRETEY(1987) Telescopus fallax ? ? ovip. 70 / 80

animals than in the Alps or in northern demonstrated that larger females attracted Europe (LUISELLI 1996). True combats be- more males than smaller ones, probably tween males were never observed by us. because of size-dependent differences in However, studies on Grass Snakes {N. na- sexual pheromone production. trix) held in both captivity (MADSEN & No comparably detailed data is avail- SHINE 1993a) and semi-natural conditions able for N. maura (LINNAEUS, 1758) and N. (LUISELLI 1996) suggest that in these tessellata (LAURENTI, 1768). Observations "mating balls" the larger males copulate on M tessellata in the Tolfa Mountains more frequently than the smaller ones be- (central Italy) suggest that courtship by cause they are more vigorous and thus multiple males (2-5 per female) occurs fre- more able to obtain a good position for quently in water: the males, usually smaller copulating. The age of the fighting males than their partner (FILIPPI & al. 1996; was not correlated with individual mating ZIMMERMANN & FACHBACH 1996), swim success both in the field and in outdoor en- around the female trying to insert their closures (LUISELU 1996). LUISELLI (1996) hemipenis into 'her' cloaca. Copulation oc- ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at Sexual behavior in Italian colubrids IH

curs when the female stops swimming, and access to females were observed on many rests almost motionless on an emerging is- occasions, usually during April when the let or on submerged grounds. Eventual de- mating season intensity peaks (CAPULA & terminants of individual reproductive suc- al. (1997). In a single case (12 April 1995; cess are completely unknown in both spe- 10.10 a. m. in European Standard Time), cies, yet concerning N. tessellata experi- five males were involved in a fight in the mental research started in 1995. In the presence of a female. The combats ap- Tolfa Mountains N. tessellata does not peared ritualized, and the males did not show an explosive mating season, and bite at one another. However, these snakes mating "balls" are less frequently found are extremely quick and ready to disappear than in N. natrix. into bushes; so we never had the opportu- Coluber. Three species belonging to nity to observe any combat for more than a this genus are found in Italy; all are ovipa- few seconds. Thus, we cannot be sure that rous and with male-larger SSD. There is no biting is not a behavioral component of obvious chromatic sexual dimorphism in these male-male fights. GUIBE & SAINT any of the Italian species of this genus. GIRONS (1955) already reported on the oc- The reproductive behavior of C. ge- currence of male-male fights in French monensis LAURENTI, 1768 is completely populations of this taxon, but did not men- unknown, because of its rarity in the Italian tion biting as a component of these inter- territory (LAPINI 1983). Ritualized combats actions. Our field observations show that between two Croatian males housed in during courtship there is intensive toungue captivity by us were frequently observed flicking between partners, with male-head- during April 1995. These males had a total noddings and body contact relatively simi- length of 106 cm and 101.5 cm, respec- lar to those described for Vipera berus tively. Their combats occurred also for food (ANDREN 1986). Copulating pairs were oc- when dead lizards or mice were put into casionally seen while basking in well- the enclosure. In general, these combats re- exposed spots, usually on dry substratum. sembled those of Lampropeltis getulus hol- A recent study carried out on free-ranging brooki STEJNEGER, 1902 (CARPENTER C. viridiflavus demonstrated that (i) adult 1977b), and the contestants did not bite females are usually able to bear every year, each other. When the males fought for food and (ii) also those unready for reproduction (n = 33 times), the larger one almost al- are attractive to males and participate in ways ended up eating the prey (81.8% of the population's sexual activity (CAPULA & the cases, X1 = 6.68, df= 1, P < 0.05), thus al. 1995). This finding may have important suggesting that body size is important for consequences for the mating system of this determining dominance in the combats be- species (see below). tween male C. gemonensis. Sexual combats The sexual behavior of the Horseshoe of male C. gemonensis were already re- Whip Snake, - Coluber hippocrepis LIN- ported by STEMMLER-MORATH (1935), NAEUS, 1758, is completely unknown, and, DAVIS (1936) and SHAW (1951). However, thus, we cannot provide any information. the behaviors of courtship and copulation Coronella: This genus consists of two have not been described in detail until now, small sized (< 80 cm long) species. Both and further research could be of value. species are characterized by minor SSD The Western Whip Snake - Coluber (CAPULA & al. 1995b) and obvious sexual viridiflavus LACÉPÈDE, 1789, is the most chromatic dimorphism (SHINE 1993). The common Italian snake but, despite this, its reproductive mode of the Smooth Snake, sexual behavior is still largely unknown. In Coronella austriaca LAUIRENTI, 1768, is the populations of Mediterranean Central live-bearing, while that of the Southern Italy (Tolfa Mountains) the above-ground Smooth Snake, C. girondica (DAUDIN, activity usually starts in March-April, the 1803), is oviparity. In both species the males emerging earlier than the females males clench their teeth on the body of the (FILIPPI 1995; CAPULA & al. (1997). In female during copulation, that may last 6-7 early spring several individuals were fre- hours (NAULLEAU 1984). quently found in close proximity to one The males of C. austriaca vigorously another, and combats between males for and cruelly combat for access to females in ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at

112 MASSIMO CAPULA & LUCA LUISELLI early spring. These combats were observed three species (Pozio 1976; FILIPPI 1995). during early April in a Mediterranean area All species of this genus are characterized of central Italy (Oriolo Romano, Tolfa by similar mating behavior (see GIL- Mountains, about 450 m a.s.l.), and during LiNGHAM 1979; BUTLER 1991). The male mid to the end of May in an alpine locality courts the female by continuously touching (Sella Nevea, Carnic Alps, about 1100 m 'her' with 'his' chin and tongue, and biting a.s.l.) where male Smooth Snakes emerge 'her' in the nape. The female responds to from winter inactivity later in April, soon this stimulation with uncoiling and after the snow cover melts (LUISELLI & al. stretching out completely, both animals 1996). In the eastern Alps the male-male showing rapid epidermic caudocephalic combats were occasionally observed under waves in this phase (see also BLASQUEZ stones, in the presence or absence of the 1994). Finally, the male inserts one hemip- females. Similar behavior was observed in enis in the female cloaca. During this Swedish Smooth Snakes (C. ANDREN, pers. phase the epidermic waves become slower. comm.). Our experiments (still in progress) The end of the mating is indicated by (1) indicate that in these combats the bigger the male releasing the female from the males win more often and drive the smaller coital bite and (2) separation of the ani- ones away from the receptive females. mals. Also in C. girondica combats be- Fights between male E. longissima tween males were observed from the end of were frequently observed in April and May April to mid-May in a Mediterranean lo- in several Mediterranean localities of cen- cality of central Italy (Tolfa Mountains, tral Italy (Tolfa Mountains, about 200-450 about 250 m a.s.l.), at the edge of spiny m a.s.l.). These fights occurred not only on bushes or under stones. In these combats the ground but also on trees and walls at the males bite their rivals vigorously but more than 3 m above the ground. The com- also use their tails for "lashing" the body of bats were highly ritualized, without biting. the enemy. The males sloughed before the As already observed by SHAW (1951), we beginning of the mating season, thus tak- noted that a high vertical stance of the ing a bright pink-orange coloration in the head, neck and anterior trunk was a fre- flanks. We are actually experimenting un- quent posture in combats of male Aescu- der semi-natural conditions to see whether lapian Snakes. Also in this species, how- bright coloration has a communication ever, it has been rather difficult to observe value, and whether the individuals with combats in nature for more than a few sec- more saturate coloration have higher mat- onds, and thus we cannot be sure that biting success than the less coloured ones (as ing is not a behavioral component of these in some lizards, see OLSSON 1994a, 1994b; male-male fights. Courtship and copulation of CAPULA & al. 1997). The concurrent pres- our captive animals was characterized by ence of male-male combats and bright dor- the typical coital biting of the male to the sal coloration suggests some convergence head or the anterior part of the body of the in traits of reproductive behavior between female; this behavior was already observed C. girondica and V. berus (see ANDREN by LOTZE (1975). As already reported for 1986; LUISELLI 1995), despite these two C. viridiflavus, in E. longissima nearly all taxa are neither phylogenetically related adult females are inseminated during the nor ecologically similar. reproductive season, although some of Elaphe: Four species of this genus are them may not be ready to produce eggs found in Italy; however, one of them - the (CAPULA & al. 1995a). The same has been Ladder Snake, E. scalaris (SCHINZ, 1822) - observed by NAULLEAU (1992) in popula- is known to occur in one locality only tions from western France. (DORIA & SALVIDIO 1994). All the species Sexual combats are components of are oviparous, with no evident colour di- the reproductive biology also of the Four- morphism between sexes. In most popula- Lined Snake - E. quatuorlineata (LACÉ- tions of the Aesculapian Snake - Elaphe PÈDE, 1789), and of the Leopard Snake - E. longissima (LAURENTI, 1768), males are situla (LINNAEUS, 1758) (see Pozio 1976, larger than females (NAULLEAU 1992), but 1983). Some male-male combats of Four- the reverse situation is found in the other Lined Snakes were observed in nature be- ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at

Sexual behavior in Italian colubrids 113

tween mid-May and the beginning of June known. The information provided here in a Mediterranean locality of central Italy comes from two adult males of Lampedusa (Rota, Tolfa Mountains, about 200 m Island that were held during spring 1996 in a.s.l.). The males were seen biting their ri- a cage of 100 x 60 cm. The males in our vals vigorously in these combats. However, cage fought several times in spring (mid- due to the very secretive habits of this spe- April), despite no female being available. cies, nothing is known on the mating be- These combats lasted for 1-3 minutes only havior of E. quatuorlineata. Copulations and were characterized by frequent biting. were observed in Mediterranean central It- Malpolon monspessulanus (HER- aly from late May to late June, usually in MANN, 1804): This large sized (up to 2.5 m the afternoon (15.30 - 19.30, see FILIPPI long, see BRUNO & MAUGERI 1990) ovipa- 1995). The behavior displayed by copulat- rous psammophine snake, shows remark- ing animals is similar to the one described able male-larger SSD and sex differences above for the whole genus Elaphe. Addi- in colour, the males being uniform and the tional information on this issue is given by females being black spotted in the dorsal Pozio (1976). parts (DE HAAN 1994). The sexual behavior of Italian E. M. monspessulanus is probably one of scalahs is completely undescribed. How- the European colubrids with a more com- ever, detailed information has been re- plex sexual and social behavior. The males ported on French and Spanish individuals. combat for access to females during the The copulatory behavior is nearly identical mating season (mid-May to early June, see to that described above for the whole genus CHEYLAN & al. 1981), and remain vigilant (BLASQUEZ 1994). The mating season lasts over the female site for a prolonged time from April to the beginning of June in (DE HAAN 1984), showing a kind of southern France (and thus, most probably "vigilance" behavior similar to that ob- in Italy as well, CHEYLAN & GUILLAUME served in V. bents (LuiSELLl 1993a, 1993b, 1993), and from 9 to 22 June in the SW 1995; MADSEN & al. 1993) and V. aspis Iberian Peninsula (BLASQUEZ 1994). (SAINT GIRONS 1996). In M monspessu- Our observations on E. situla come lanus the copulation can be voluntarily in- from three captive specimens only (two terrupted and quickly recommenced due to males and a female) maintained in an out- the peculiar structure of the male hemipe- door terrarium of 180 x 60 cm. In this en- nis (DE HAAN 1984). M. monspessulanus is closure the bigger male (77 cm long) also known for a kind of "rubbing" head fought repeatedly with the smaller one behavior (DE HAAN 1982) which may serve (68.5 cm long) during spring (March and for habitat and congener marking with April), excluding it from copulation with chemical substances (DE HAAN 1993). the female available. The combats were Telescopus fallax (FLEISCHMANN, similar to those of E. longissima in some 1831): This is one of the very rare species postures (SHAW 1951), but bites and pro- of Italy (LAPINI 1983), and its sexual be- longed pursuits were usual components of haviors are nearly unknown. It is not clear these fights. Some fights were very violent; whether the males combat for access to fe- the smaller animal in our cage finally died males, and data on reproductive seasonality after about two months of continued ag- is very scarce and anecdotal (BRUNO & gressive actions through the stronger male. MAUGERI 1990). Coloration features are It is interesting to note that aggressive be- similar in the sexes (BRUNO & MAUGERI havior did not only occur for access to the 1990), despite ZINNER (1985) reported on female, but also in competing for food. remarkable sex differences in colour in its Macroprotodon cucullatus (GEOFF- congener T. dhara (FORSKAL, 1776). The ROY, 1827): The sexual behavior of this females are generally larger than males very elusive species is still completely un- (BRUNO & MAUGERI 1990). Alternative reproductive strategies and the potential for long-term sperm storage The climatic types of the Italian Pen- various regions and include the typical insula are rather diverse depending on the Mediterranean climate (in coastal, central ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at

114 MASSIMO CAPULA & LUCA LUISELLI and southern Italy), the subcontinental Ap- natrix emerges from hibernation in late ennine climate (in the Apennines and in April (males earlier than females), copula- the Sardinian and Sicilian mountains), the tion takes place in May, opposition in the subcontinental temperate Adriatic climate second part of July, and eggs hatch at the (in the Adriatic coast), the continental cool- end of August. C. austriaca also emerges temperate climate (in the Po river plain), from hibernation in late April (males ear- and the continental cold Alpine climate (in lier than females) and has its mating sea- the Alpine regions) (ACCORDI & LUPIA son in May, but gives birth to young in late PALMIERI 1979). Despite this relative vari- August or at the beginning of September. ety of mesothermic climates, all the Italian Spring mating (more or less immediately snake species show a similar reproductive after the end of hibernation, depending also seasonality, primarily determined by the on the proximate climatic conditions), length of the hibernation phase and by the early summer oviposition and late summer reproductive mode. The reproductive sea- hatching are, with minor local and species- sonality of the Italian colubrids is well ex- specific differences, widespread patterns in plained by that ofN. natrix and C. austria- Italian colubrids (see AGRIMI & LUISELLI ca in the eastern Alps (see LUISELLI & al. 1994 for C. girondica, and CAPULA & al. 1996, 1997). The former species can be 1995a for C. viridiflavus and E. longissi- used as a model for describing the repro- ma). The possibility of finding alternative ductive seasonality of the oviparous snakes, reproductive strategies in Italian colubrids the latter for the live-bearing snakes. N. is thus very limited. Spring births in cold (high-altitude) climates

From a locality of the extreme south- (CAPULA & al. 1995b, and unpublished ob- ern tip of Sweden, MADSEN (1989) repor- servations; LUISELLI & al. 1996, 1997). ted on the very rare event of a female V. Twenty-eight C. austriaca females studied bents giving birth in spring (11th April in the eastern Italian Alps (Tarvisio Forest, 1988), despite young are usually born from province of Udine) for a period of five August to early September in this species years (obtaining an average of 1.07 ± 0.60 (NILSON 1981; CAPULA & al. 1992). litters each, with a range of 0 to 3) gave MADSEN suggested that (i) this event was birth in late summer and did not show any most likely caused by the cold summer in significant annual variation in the dates of 1987, and (ii) the female which gave birth parturition (examining year- to-year varia- in spring had to enter hibernation while tion by one-factor ANOVA with year as the still gravid and the embryos were able to factor: F4,22=0.25, P=0.9), and the same survive the hibernation period. He finally was true for 20 N. natrix females of the hypothesized that spring birth could be an same geographic area which oviposited al- alternative reproductive strategy in areas ways between 17 and 30 July without any with shorter activity seasons for snakes at year-to year difference (one-factor ANOVA northern latitudes and / or high altitudes. with year as the factor: F3, ]0 = 1.48, P = This alternative reproductive strategy 0.28). Moreover, 100% of the gravid fe- was never observed in Alpine Adder males of N. natrix (n=ll), C. viridiflavus populations from the higher elevations (w=3) and C. austriaca (w=8) inhabiting a (2200-2500 m a.s.l., see CAPULA & LUISEL- mountain area of the central Apennines LI 1992), and seems not to occur in the (Velino Massif, about 1500 m a.s.l.) ovi- Italian colubrids, including both live- posited in late July (oviparous species) or bearing and oviparous taxa. In this regard gave birth to young at the beginning of we have detailed data for two alpine popu- September (live-bearing species), showing lations of colubrids, and also some obser- no remarkable difference with conspecifics vations for populations inhabiting the Ap- from other geographic areas. Thus, our ennine massif. In the Alpine cool climate current data does not support MADSEN'S populations of C. austriaca and N. natrix (1989) hypothesis, although more data on all gravid females gave birth in late sum- high mountain populations of snakes is mer, without remarkable variations among required before firm statements can be individual females or among research years made. ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at

Sexual behavior in Italian colubrìds 115

Autumnal mating and long-term sperm storage

In several reptile species there may be which constrain the snakes to retire into long preservation of spermatozoa in the hibernation before the end of October genital organs (usually in the vaginal seg- (LUISELLI & al. 1996, 1997). On the other ment of the oviduct) of females (SAINT hand, an autumnal mating season is likely GIRONS 1973). Theory suggests that sperm to occur in the Mediterranean regions storage may evolve to secure reproduction where the mild climate permits prolonged in populations or species having weakly autumnal activity of snake populations pronounced mating seasons (e. g., in tropi- (until end of November or early Decem- cal species with irregular and "unsyn- ber). However, despite careful research chronized" mating periods) and low densi- over several years (1985-1995), no autum- ties (PORTER 1972). In European snake nal copulation was seen in most of the species long-term sperm storage is rare and colubrids of Mediterranean central Italy, restricted to populations showing not only including N. natrix, N. tessellata, E. long- the usual spring mating season but also a issima, E. quatuorlineata, C. girondica, less intense autumnal mating season (e.g., and C. viridißavus (AGRIMI & LUISELLI some populations of V. aspis, V. seoanei 1994; CAPULA & al. 1995a, 1995b; FILIPPI and V. latastei; see SAINT GIRONS 1976). 1995; CAPIZZI & al. 1996). On the other Thus, long-term sperm storage is not ob- hand, the occurrence of autumnal copula- served in V. berus and other species exclu- tions was occasionally observed in C. aus- sively mating during springtime (ANDREN triaca: a mating pair was seen in Oriolo & NILSON 1987; LUISELLI 1993b, 1995; Romano (Tolfa Mountains, province of HOGGREN & TEGELSTROM 1996). Viterbo, about 450 m a.s.l) on October 17, Literature data on the occurrence of 1989, and another mating pair in the same long-term sperm storage in European locality on October 3, 1995. In these two snakes is still very scarce. To our knowl- cases the females were not collected, and it edge, solely PARELLADA (1995) reported on was thus impossible to establish whether a snake population (V. latastei) in which autumnal copulations effectively resulted in copulation was not observed in spring but their fecundation. A true case of long-term only during autumn, thus indicating ob- sperm storage was observed in N. maura: ligatory use of sperm storage as a repro- one out of five adult females collected ductive strategy. However, this author's ob- during late October 1992 in a locality in servations were done in an outdoor enclo- central Sardinia (Giara di Gesturi, about sure with relatively little evidence of simi- 270 km southwest of Nuoro, 550 m a.s.l) lar phenomena occurring in nature. In all oviposited on 3rd July 1993, despite no other cases reported, sperm storage appears male has been housed in the terrarium. to be merely an anomalous event linked to This female was 58.3 cm long, its clutch autumnal mating (SAINT GIRONS 1973). size was 7 eggs, and the mean egg size was This was the case, for instance, in some 27.8 x 15.9 mm, which is much smaller individuals of C. austriaca (DUGUY 1961), than that of the eggs deposited by other N. M. maura (DUGUY & SAINT GlRONS 1966), maura which mated in spring (x = 29.6 x and N. natrix (D'ABADIE 1928;.NAULLEAU 16.8 mm, n = 135 eggs). Moreover, only 1984). These two latter species are also one offspring hatched; it was born on known for some cases of exceptionally August 7, 1993 (35 days after oviposition), prolonged sperm survival in the female measured 17.2 cm in total length and was uterus (six years according to QUILLON & in excellent health condition. LAMOUILLE 1978). Recent field-work demonstrated that Careful field studies excluded the oc- in a locality of Mediterranean central Italy currence of sperm storage in Alpine popu- (Tolfa Mountains, province of Rome) most lations of N. natrix and C. austriaca from of the female C. viridißavus and E. longis- the Tarvisio Forest (about 1100 m a.s.l.) sima are inseminated during the intense (LUISELLI & al. 1996, 1997). In this region spring mating season, although some of an autumnal mating season is unlikely to them are unready to produce eggs (CAPULA occur due to the low ambient temperatures & al. 1995b). This finding, which is ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at

116 MASSIMO CAPULA & LUCA LUISELU probably valid for many other populations But now we have much more data at hand. of European snakes (ANDREN & NILSON To test females for the occurrence of sperm 1987; NAULLEAU 1992; LUISELLI 1993B; storage, we housed several inseminated SAINT GIRONS 1996), is particularly rele- specimens from our previous study in ter- vant because it introduces a potential for raria for a period of at least 365 days with- long-term sperm storage in these animals. out males (see LUISELLI 1993b for an iden- One could hypothesize that these insemi- tical experimental procedure with V. be- nated females, unable to ovulate and pro- rus). None of these females (8 E. longis- duce eggs within-season, could preserve sima and 7 C. viridiflavus) produced eggs sperm in their genital organs. Ova could the year following insemination, despite then be fertilized in the following year(s), their body condition being fit for reproduc- when the female's body fat reserves neces- tion (BCI > 0.55, see NAULLEAU 1992) due sary for reproduction will have finally re- to substantial feeding on laboratory mice. stored. When we submitted the original Thus, we are led to conclude that these CAPULA & al. (1995a) paper for publication within-season inseminated non-reproduc- (October 1994), we did not have enough tive females do not keep sperm in their data to draw firm conclusions on this issue, genital organs. and thus preferred to avoid any discussion.

DISCUSSION

Sexual fights among males were seen ("type 1") occurs in 8 species (four viperids in 13 snake taxa (68.4% of the Italian and four colubrids), while "type 2" is typi- snake fauna) and 21 populations. This pro- cal to two species (C. austriaca, M. cucul- portion should probably be retouched be- latus), "type 3" to one species (C. giron- cause we had no available information on dica) and "type 4" to two Elaphe. Interest- three very rare species. The sole taxa that ingly, "type 2" is present in two taxa that, seem to lack sexual fights are those of the although phylogenetically unrelated, have genus Natrix, which are also the sole semi- semi-fossorial habits and convergent mor- aquatic snake species of Italy (BRUNO phological traits (WADE 1988; BUSACK & 1984; LUISELLI & RUGIERO 1991; FILIPPI MCCOY 1990; PLEGUEZUELOS & al. 1994). 1995). However, at least in one of these Biting is present only in non-venomous species (N. natrix) physical interactions species (genera Coronella, Elaphe and Ma- between males simultaneously courting croprotodon); this also agrees with SHINE'S single females may lead to a kind of (1994) conclusions. The combats we as- "pseudocombat" where male body size is sisted at were all harmless to the rivals, ex- important for increasing the individual re- cept those of E. situla which were occa- productive success (MADSEN & SHINE sionally so cruel that a captive male in our 1993; LUISELLI 1996). Sexual combats cages killed a smaller contestant. This were found in species where males are big- should be considered as one of a few cases ger than females (n = 5), in species with of male-male combat departing considera- minor SSD (ji = 4), and in species with bly from the typical highly ritualized significantly reversed SSD (n = 4). Exclud- dance, thus, resulting in combat fatality ing the three species for which data are not [see also PERRY-RICHARDSON 1991, for available, 100% of the taxa with minor Chondropython viri dis (SCHLEGEL, 1872)]. SSD or with male-larger dimorphism Interestingly, whilst sexual combats were showed sexual combats, but only 57.1% of omnipresent in the live-bearing taxa (n = 5 those with reversed SSD. This considera- species, 100% of the cases), the same ago- tion empirically supports the conclusion nistic behavior was present only in 72.7% that male-larger dimorphism and occur- of the oviparous ones (w = 11 species). rence of sexual combats are correlated in Moreover, sexual combats were exhibited snakes (SHINE 1978, 1993, 1994). both by alpine and Mediterranean snake Ritualized combats without biting populations (see table 1). ©Österreichische Gesellschaft für Herpetologie e.V., Wien, Austria, download unter www.biologiezentrum.at

Sexual behavior in Italian colubrìds 117

ACKNOWLEDGMENTS We thank Dr U. AGRIMI (Istituto Superiore di borg, Sweden) for other sources of original data. Miss Sanità, Rome) who provided data on Elaphe si tula, Dr. JANE TANTON (Southampton, UK) improved the English E. FILIPPI, Dr. V. TRUJILLO JESUS (University of Rome of this article. Financial funds for this study were pro- "La Sapienza") and Dr. C. ANDREN (University of Göte- vided by the Italian M.U.R.S.T. and C.N.R. (40%).

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DATE OF SUBMISSION: April 3rd, 1997 Corresponding editor: Heinz Grillitsch

AUTHORS: Prof. Dr. MASSIMO CAPULA, Museo Civico di Zoologia, viale del Giardino Zoologico 20, 1-00197 Rome, Italy; Dr. LUCA LUISELLL Department of Animal and Human Biology, University of Rome "La Sapi- enza", via Alfonso Borelli 50,1-00161 Rome.